Abstract
Despite over 100 years of digenean trematode parasite species descriptions, from a wide diversity of vertebrate and invertebrate host species, our ability to recognize the diversity of trematode species within a single lake remains an incredible challenge. The most challenging aspect is the identification of species from larval stages derived from intermediate hosts, due to the disjointed data of adult worm morphological descriptions, from which species are named, and links to corresponding molecular identifiers in depauperate databases. Cryptic species also play a significant role in the challenge of linking trematode larvae to adults, species identifications, and estimating diversity. Herein, we utilize a large, longitudinal dataset of snail first‐intermediate host infection data from lakes in Alberta, Canada, to infer trematode larval diversity using molecular phylogenetics and snail host associations. From our assessments, we uncover a diversity of 79 larval trematode species among just five snail host species. Only 14 species were identified to a previously described species, while the other 65 species are either cryptic or otherwise unrepresented by mitochondrial genes in GenBank. This study currently represents the largest and most diverse singular molecular survey of trematode larval fauna composed of over one thousand mitochondrial sequences. Surprisingly, rarefaction analyses indicate we have yet to capture the complete diversity of trematodes from our sampling area.
Keywords: Alberta, cercariae, digenea, diversity, phylogenetics, trematoda
1. INTRODUCTION
Trends in the ecology of pathogens are reliant upon an accurate identification of both pathogen and host species. However, the precise identification of endoparasites can be precarious, due to the lack of hard, morphological structures that arthropod ectoparasites have (Mathison & Pritt, 1997). Furthermore, larval and immature endoparasites often lack reproductive structures used to identify their adult counterparts. Both of these problems are common among helminths (Jensen & Bullard, 2018; Roeber, Jex, & Gasser, 1998; Schell, 2009). Additionally, the revelation of cryptic species is becoming more common, as molecular methods expose diversity not identifiable by traditional, morphological methods (Detwiler, Bos, & Minchella, 2016; Detwiler, Zajac, Minchella, & Belden, 2013; Georgieva, Selbach et al., 2001; Herrmann, Poulin, Keeney, & Blasco‐Costa, 1993a; Locke, McLaughlin, Dayanandan, & Marcogliese, 2010; Miura, Kuris, & Torchin, 2003; Nadler & León, 2016; Pérez‐Ponce de León & Poulin, 2010b). Finally, there is a lack of general survey data on parasites, causing gaps in our understanding of diversity and richness for defined geographical locations (Adlard, Miller, & Smit, 1998; Adlard & O'Donoghue, 2015; Mollaret et al., 2015). Taken together, plastic and cryptic morphology, with a lack of survey data, makes it more difficult to correctly identify a parasite sample from a new location.
Recent meta‐ and spatial analyses have shown that our understanding of parasite diversity is biased toward location, time, and parasite class, correlating with when and where taxonomists are most active during their careers, and it is argued that more taxonomists are needed (Poulin, 2011; Poulin & Jorge, 2018). Molecular methods have come a long way in allowing faster and more precise species identifications and the ability to make hypotheses about species relationships and evolution considering cryptic morphology. However, even with these methods, regional checklists of host–parasite relationships remain incomplete (Poulin, Besson, Morin, & Randhawa, 2015). One major issue is depauperate and biased databases, directly related to research and funding interests, expertise, and the natural evolution of improving methodologies over time. So, not only do we need more taxonomists, but we need them to study more broadly to fill in these gaps in our understanding of parasite diversity.
Ecologically speaking, most parasites have incomplete life cycle descriptions. Likewise, our understanding of their distributions and interactions within and among host species is limited due to a lack of surveillance records and repeated or long‐term studies. The dispersion of parasite data constrains our knowledge of the finer details of their ecology across broad geographic ranges. Additionally, unreliable morphological assessments in survey data present the caveats that (a) the species identities may not be accurate and (b) the survey may not represent true diversity within the area, missing cryptic species all together and underestimating overall diversity. Furthermore, the onset of molecular methods for species identifications has widened the knowledge gap through revelations of prior undetected diversity that cannot always be traced to a described species. In fact, the revelation of cryptic species is enhanced with greater sequencing effort, and more so for trematodes than any other group of parasitic helminth (Pérez‐Ponce de León & Poulin, 2010b). This, overall, can make it incredibly difficult to understand the larger picture when it comes to parasite ecology because we are lacking long‐term, field studies, and precision in data collection.
Digenean trematodes are a very large group of parasitic helminths, with complex life cycles. The adult worms infect vertebrate hosts, in which their eggs are passed into the environment with the feces of the animal. The eggs hatch and infect a snail (or other mollusk), in which their larval development occurs. Larvae will emerge from their obligate, snail, first‐intermediate host to then infect either a second‐intermediate host or a definitive host, depending on the species. Current estimates for the number of trematode species range from 18,000 (Cribb et al., 2016) to 24,000 (Poulin & Morand, 2014).
Traditionally, taxonomic descriptions of trematodes are from morphological traits of adult worm stages derived from vertebrate hosts, as their most prominent features are fully developed and measurable, contrasting the less developed features of the larval stages (Schell, 2009). With the onset of molecular barcoding, not only have we realized the problems of cryptic morphology and the need for multiple lines of evidence for species delineation, but that for trematodes, we can now use larval stages to delineate species (Detwiler et al., 2016, 2013; Georgieva, Selbach et al., 2001; Gordy, Locke, Rawlings, Lapierre, & Hanington, 2013b; Locke, Mclaughlin et al., 2010; Schwelm, Soldánová, Vyhlídalová, Sures, & Selbach, 2011; Soldánová et al., 2014). This is advantageous in that it is considerably easier to collect larvae from snail, first‐intermediate hosts. The disadvantage is the lack of a direct connection between adult morphological records and molecular records.
The goal of this study was to capture an accurate identification of the trematode biodiversity among snail first‐intermediate hosts to establish a better, ecological understanding of trematode communities and how they differ geographically and change over time. In this study, we use molecular phylogenetic methods to assess species relationships, to identify collected specimens, and account for possible cryptic morphology. Snails and trematodes were collected from six lakes in central Alberta, Canada, over 3 years, from June to September. This longitudinal dataset provides novel contributions to the species diversity of trematodes, new geographical species records in central Alberta, and snail host association records, to better connect trematode life cycles. Though the data collected for this study were a continuation of our previous long‐term dataset (Gordy, Kish, Tarrabain, & Hanington, 2013a), the use of phylogenetic methods herein both expand and improve upon our understanding of trematode diversity and clarify identification issues we confronted previously.
Several trematode families have previously been given a considerable amount of attention in molecular phylogenies, more than others (e.g., Diplostomidae and Echinostomatidae). Therefore, species delimitation methods and acceptable sequence divergence limits have been tested for specific genes within these, well‐studied, trematode families (Blasco‐Costa & Locke, 2011; Detwiler et al., 2013; Georgieva et al., 2012; Georgieva, Selbach et al., 2001). Most trematode families have not been given such attention. Though there are general assumptions extrapolated from previous studies, such as 5% sequence divergence of cytochrome c oxidase subunit 1 (cox1) as an acceptable limit for species delimitation (Vilas, Criscione, & Blouin, 2014), this remains to be tested for all trematode families. Herein, we test this 5% assumption for delimitation using cox1 across seven trematode families.
The resulting diversity estimates from this study exemplify both the power and utility of molecular phylogenetics for species identification, but this study also identifies gaps and caveats that trematode taxonomists may face in future studies. Therefore, we provide commentary on the current caveats of the field of trematode taxonomy, cryptic species, depauperate databases, and areas in need of further research. We also provide a current record of trematode and host associations within Alberta and encourage the continued effort to better understand trematode diversity from both a regional and global context.
2. METHODS
2.1. Trematode and snail sample collection and selection
As a continuation of the 2‐year survey described in Gordy et al. (2013a), snails were collected for an additional year in the same manner from the following sites: Lake Isle, Lake Wabamun, Gull Lake—Aspen Beach, and Buffalo Lake—Pelican Point, Rochon Sands, and The Narrows (Figure 1). All methods regarding collection and sample processing, including molecular methods, were the same as previously described (Gordy et al., 2013a, 2013b).
Figure 1.
Sample collection locations. Map of the six lakes from which snails and trematodes were collected in central Alberta, Canada. Depth of lake is given as a mean depth in meters
Briefly, snails were collected from sites previously established and brought back to the laboratory for examination of patent infection by larval trematodes. Trematode infections, when patent, resulted in larval cercariae emerging from the snail into the surrounding water. Free‐swimming cercariae were detected with a dissecting microscope, collected from the sample well, and preserved for downstream molecular work. Our original aim was to extract DNA and barcode every parasite sample. However, with over 2,400 samples, this goal was not feasible in cost and time. Nearly half the trematodes derived from the total collection were xiphidiocercariae, and previous sequencing efforts revealed these samples to be closest to Plagiorchis sp. (Gordy et al., 2013a). Therefore, much of the sequencing efforts went to all other morphotypes for which there were enough cercariae available for sequencing (i.e., >10 cercariae, to keep a voucher stored in ethanol). For cost feasibility, we chose to sequence only 70 haphazardly sampled xiphidiocercariae samples, representative of sites and snail host species from which they were found. The sequencing effort strategy for all other morphotypes was complete coverage.
2.2. DNA isolation, sequencing, and analysis
DNA was extracted from cercariae preserved in 50% RNAlater or 95% ethanol, as previously described (Gordy et al., 2013a). The partial NADH dehydrogenase subunit 1 (nad1) mitochondrial gene was sequenced for all cercariae for which morphological characterization or previous mitochondrial cox1 sequencing attempts (Gordy et al., 2013a) placed them in the family Echinostomatidae. Because of high saturation within the cox1 gene for this family, nad1 has been the gene of choice in the literature (Detwiler et al., 2016, 2013; Georgieva et al., 2012; Morgan & Blair, 2015) and best represented the samples within GenBank for comparisons. For all other families, partial cox1 was used (Gordy et al., 2013a, 2013b; Moszczynska, Locke, McLaughlin, Marcogliese, & Crease, 2016; Van Steenkiste, Locke, Castelin, Marcogliese, & Abbott, 2018). Nucleotide sequence inspection, trimming, alignments, model testing for best‐fit substitution models, and maximum‐likelihood (ML) and Bayesian inference (BI) phylogenetic analyses were as described in Gordy et al. (2013b). Model testing, utilizing BIC scores for determining best‐fit, was implemented in MEGA7 (Kumar, Stecher, & Tamura, 2012). All BI analyses were run in the MrBayes (Huelsenbeck & Ronquist, 2010) plugin with chain length 10,000,000, subsampling frequency 100,000, four heated chains (chain temp 0.2), and burn‐in length of 1,000,000. All ML analyses were run with the PhyML plugin (Guindon et al., 2018), estimating parameters, and with 1,000 bootstrap iterations. All molecular analyses were run using Geneious version 11 (http://www.geneious.com, Kearse et al., 2014).
Phylogenies were first constructed using a broad sampling of taxa within each family. Sequences of the same gene (either cox1 or nad1) were gathered from each species available in GenBank within that family. Because there are no standard methods yet employed for molecular taxonomic analysis within the Digenea, and much sequencing effort has been based on personal preference, we were unable to consistently attain a good representation of the species or even genera for several families, including Psilostomidae, Notocotylidae, and Plagiorchiidae. Because of issues with substitution saturation at broader taxonomic groupings for some families, their phylogenies were further refined into either genera or groups of closely related genera that were previously published as such (e.g., Hypoderaeum is paraphyletic to Echinoparyphium within the family Echinostomatidae (Detwiler et al., 2016; Kostadinova & Herniou, 2014)).
Phylogenies were constructed at a family‐level with nonredundant sequences to understand species relationships. These family‐based phylogenies were used as a benchmark for later phylogenies, in which redundant sequences were included for identification of individual sequences (specimen samples). Because there were many sequences, some phylogenies were divided to reduce the computation time (i.e., Strigeidae, Diplostomidae, and Echinostomatidae). We only present the information relevant to species identification phylogenies below, as the species relationships were the same as those within the nonredundant family‐level phylogenies.
2.3. Species delimitation
Trematode samples were first separated by gross morphology, evidenced by previously published larval trematode descriptions (Schell, 2009). Then, percent nucleotide identities by tBLASTn (Altschul, Gish, Miller, Myers, & Lipman, 1990), phylogenies from the literature where available (Blasco‐Costa, Poulin, & Presswell, 1977; Detwiler et al., 2016; Gordy et al., 2013b; Hernández‐Mena, García‐Varela, & Pérez‐Ponce de León, 2017; Locke, Mclaughlin et al., 2010), and species names given to the sequences in GenBank to which they most closely matched from BLAST results were used to group samples into trematode families and hypothesized genera.
After phylogenetic analyses, because many of our sequences were not directly within monophyletic groups of previously identified species, we employed additional tools to further distinguish taxa. The web app, Automatic Barcode Gap Discovery (ABGD; Puillandre, Lambert, Brouillet, & Achaz, 2005), was used in combination with a priori assumptions of a 5% cutoff in sequence divergence for species delimitation using p distances calculated in MEGA7 (Gordy et al., 2013b; Kumar et al., 2012). For ABGD, nucleotide alignments were inserted and tested using all three distance measurements (Jukes‐Cantor, Kimura 2.0, and simple distance) to look for agreements on grouping and prior maximal distance, using the default minimum slope of 1.5. Other specific methods will be described separately for each trematode family below. The one family that was included in downstream diversity analyses, but not described below is the Schistosomatidae because their phylogeny from this dataset was described and previously published (Gordy, Cobb, & Hanington, 2012).
2.3.1. Family Notocotylidae
A final alignment of 98 cox1 sequences with a length of 327 bp was used for phylogenetic analyses. Echinostoma hortense (KR062182) was used as an out‐group because of its prior demonstrated phylogenetic relationship to the notocotylid Ogmocotyle sikae (KR006934.1; Liu et al., 2001), which was one of only two sequences from GenBank we were able to use for comparison. The E. hortense sequence did cause one small gap in the final alignment. Only O. sikae and Notocotylus sp. BOLD (KM538104) were used for comparison to the 95 sequences from this study, due to a lack of Notocotylid cox1 sequences available with significant overlap. HKY + G was the best substitution model and was used for phylogenetic analyses.
2.3.2. Family Psilostomidae
A cox1 nucleotide alignment was made for 11 sequences, six from this study and five from GenBank, for a final length of 498 bp. Echinochasmus japonicus (NC_030518) was used as the out‐group for phylogenetic analyses because of its previously demonstrated relationship outside of Psilostomidae, but within the superfamily Echinostomatoidea (Tkach, Kudlai, & Kostadinova, 2015). Three other species were used for comparison, namely Sphaeridiotrema globulus (GQ890329), S. pseudoglobulus (GQ890328 & FJ477222), and Pseudopsilostoma varium (JX468064). HKY + G was the best‐supported nucleotide substitution model and was used for phylogenetic analyses. Because there were so few sequences, and therefore groups of species, ABGD was not utilized for confirmation.
2.3.3. Family Haematoloechidae
A final nucleotide alignment consisted of seven sequences, one from Plagiorchis sp. (FJ477214) as the out‐group, two from GenBank (KM538096–KM538097: Haematoloechus sp. BOLD), and four from this study. The Plagiorchis sequence was used as the out‐group, based on previous use as such for phylogenies of Haematoloechidae sequences (Snyder & Tkach, 2015). The alignment was 469 bp with a few short gaps due to the out‐group sequence. HKY + G + I was the best‐supported nucleotide substitution model.
2.3.4. Family Plagiorchiidae
A final nucleotide alignment of 56 cox1 sequences was 437 bp in length. A sequence for Haematoloechus sp. (KM538096) was used as the out‐group (for reasons previously specified). Model test results showed the best nucleotide substitution model was HKY + I, which was utilized in BI and ML analyses.
2.3.5. Family Echinostomatidae
Though nad1 was the primary gene of interest for this family, based on previous work, many samples from this study were first (or only) analyzed using cox1 sequences. To resolve the issue of having some samples of one gene and some of another, sequencing of both genes for a few samples was done to make the link between gene trees. The only successful sequences from this attempt were from isolates MGC16B, MGC1214, and MGC1665. These sequences allowed the comparison between nad1 and cox1 phylogenies.
An alignment was made for all echinostome cox1 sequences from this study along with those gathered from GenBank to represent as many species as available and that covered the same region of the gene. The final alignment included 113 sequences and was 391 bp long. Two sequences for Euparyphium capitaneum (KY636235–KY636236) were used as the out‐group (Tkach et al., 2015). From GenBank, sequences from the genera Drepanocephalus, Hypoderaeum, and Echinostoma were included in the alignment, as those were all that were available. Sequences included in the alignment from this study were from the genera Echinoparyphium and Echinostoma, and while there were no reference sequences within certain clades, there was overlap from the nad1 gene tree to confirm the identity of these clades. The best‐fit model was GTR + G for both genes and for all genera within this family. The nad1 phylogenies were split into multiple groups as discussed below.
Drepanocephalus
The final nucleotide alignment (nad1) was 390 bp and included two Drepanocephalus auritus (KP053262 and KP053263) sequences, one Drepanocephalus sp. (KP053264), two unknowns from the current study (MGC2147 and MGC2353), and a Fasciola hepatica (KT893744) sequence as the out‐group. Minor gaps were present between base pairs 180 and 190 where F. hepatica has a couple base pair differences. Because there were so few sequences, ABGD was not used for confirmation.
Neopetasiger
The final nucleotide alignment (nad1) of 21 sequences was 313 bp in length, and minor gaps occurred between base pairs 108 and 116 due to F. hepatica (KT893744), which was used as an out‐group for this alignment.
Echinostoma
A final nucleotide alignment (nad1) of 73 sequences was 386 bp long and included 31 unknown sequences from this study and all available species with significant overlap in the same region from GenBank. As in Soldánová et al. (2017), among others, Isthmiophora melis (AY168948) was used as an out‐group.
Echinoparyphium/Hypoderaeum
The final nucleotide alignment for nad1 was 304 bp, with some minor gaps at position 81, 84, and 298, due to the out‐group, and included 262 sequences. Once again, I. melis was used as an out‐group. Both Hypoderaeum and Echinoparyphium sequences were included in this alignment, because previous phylogenies have shown them as paraphyletic (Detwiler et al., 2016).
2.3.6. Superfamily Diplostomoidea
Family Diplostomidae
Based on recent phylogenies by Hernández‐Mena et al. (2017), and to reduce the overall size of the analysis, the Diplostomidae were divided into two groups for phylogenetic analyses utilized for identifications. Diplostomidae‐I included the genera Austrodiplostomum, Tylodelphys, and Diplostomum and resulted in a final nucleotide alignment of 197 sequences at 347 bp, using Ornithodiplostomum scardinii (KX931425) as out‐group. Diplostomidae‐II included the genera Bolbophorus, Posthodiplostomum, Ornithodiplostomum, Neodiplostomum, and Alaria, with a final alignment of 104 sequences at 317 bp and using Crocodillicola pseudostoma (MF398317–MF398318) as the out‐group. For both groups, GTR + G + I was the best substitution model and used for phylogenetic analyses.
Family Strigeidae
Like the Diplostomidae, the Strigeidae were divided into two groups for analyses and named after the ordering found in Hernández‐Mena et al. (2017). Strigeidae‐I included the genera Cardiocephaloides, Cotylurus, and Ichthyocotylurus. The final alignment was 356 bp long and included 152 sequences. Tylodelphys scheuringi (FJ477223) was used as the out‐group for phylogenetic analyses. Strigeidae‐II included genera from Apatemon and Australapatemon, with Apharyngostrigea spp. as the out‐group (HM064884–HM064885, JX977777, & JF769451). The final nucleotide alignment was 392 bp and included 313 sequences. The best nucleotide substitution model for the Strigeidae was HKY + G + I and used in all phylogenetic analyses.
2.4. Richness and recovery calculations
The following packages were utilized in R version 3.4.3 (R Core Team, 1997) to calculate richness and diversity metrics and plot them: vegan (Oksanen et al., 2010a) and dplyr (Wickham, François, Henry, & Müller, 2016). Species richness was derived using the diversityresult (vegan) command to add unique species by site as well as pooled species richness for all sites, by snail species, and to view how they were represented by lake. Species accumulation and rarefaction were analyzed using the specaccum (vegan) command, utilizing the “collector” method to derive site richness in the order the data were collected and the “rarefaction” method to view an individual‐based, rather than site‐based, method for species accumulation, respectively. An Arrhenius nonlinear model was fit to a species accumulation curve to view the species–area relationship utilizing the specaccum with “random” method and fitspecaccum (vegan) commands. If we assume that morphological identification of larval trematodes gives the greatest confidence at the taxonomic scale of family, we predict that accumulation curves will plateau faster than with information derived from molecular phylogenetic identifications that can provide confidence to the species‐level. To show this, we repeated the same accumulation and rarefaction analyses at the level of trematode family. This process was repeated for snail species, with exception of the Arrhenius nonlinear model, which would not converge.
3. RESULTS
A total of 17,447 snails were collected over the 3‐year period across all 11 sites (Figure 1 and Table 1). Snail species abundances are as follows: Stagnicola elodes = 9,505 (54.48%), Lymnaea stagnalis = 516 (2.96%), unidentified lymnaeid = 2,252 (12.91%), Helisoma trivolvis = 1,166 (6.68%), Planorbula armigera = 1 (0.01%), unidentified planorbid = 143 (0.82%), and Physa gyrina = 3,864 (22.15%). Of these collections, only 2,452 (14%) snails carried patent trematode infections, meaning cercariae were actively emerging from the snail. Unidentified lymnaeids and planorbids mentioned above were all uninfected. Most infections were found among S. elodes snails (1,892/77.16%), followed by P. gyrina (354/14.44%), L. stagnalis (123/5.02%), H. trivolvis (82/3.34%), and finally P. armigera (1/0.04%). Of these infections, 1,149 (46.8%) were classified as xiphidiocercariae by morphology (by having a clearly defined stylet in the anterior rim of the oral sucker (Schell, 2009)).
Table 1.
Counts of snail species by collection site
| Buffalo Lake—Pelican Point | Buffalo Lake—Rochon Sands | Buffalo Lake—The Narrows | Gull Lake—Aspen Beach | Isle Lake | Lac La Nonne | Lac La Nonne site #2 | Pigeon Lake—Provincial Park | Wabamun Lake—Provincial Park Beach | Grand total | |
|---|---|---|---|---|---|---|---|---|---|---|
| Helisoma trivolvis | – | – | 145 | 4 | 202 | 123 | 23 | – | 669 | 1,166 |
| Lymnaea stagnalis | 1 | – | 462 | 28 | 1 | – | – | – | 24 | 516 |
| Physa gyrina | 209 | 257 | 329 | 195 | 831 | 138 | 324 | 4 | 1,577 | 3,864 |
| Planorbula armigera | – | – | – | – | – | – | – | – | 1 | 1 |
| Stagnicola elodes | 3,567 | 368 | 36 | 399 | 3,457 | 1,179 | 370 | – | 129 | 9,505 |
| Unidentified lymnaeid | – | – | – | 1,192 | – | – | – | – | 1,060 | 2,252 |
| Unidenitifed planorbid | – | – | 78 | 7 | 1 | – | – | – | 57 | 143 |
| Grand Total | 3,777 | 625 | 1,050 | 1,825 | 4,492 | 1,440 | 717 | 4 | 3,517 | 17,447 |
A total of 1,091 trematode cercariae samples were successfully extracted and sequenced for downstream molecular phylogenetic analyses. Less than 200 cercariae samples, excluding xiphidiocercariae, were not included in the final diversity analyses, either because of low quantities of cercariae, low quantity or quality of DNA, or bad sequencing results. Phylogeny results will be discussed in the same order as above, by family, in the sections below.
Several new lineage and singletons have emerged from these phylogenies, and we refer to them below as “species.” We acknowledge the limitations of using molecular phylogenies for species identifications, without further supporting evidence (e.g., sequences from adult specimens) and that others would refer to them as operational taxonomic units (OTUs). However, we prefer to use the term species to remain consistent with our previous publications and sequence names.
3.1. Family Notocotylidae
Despite there being 19 different species represented in GenBank from the superfamily Pronocephaloidea, only five species had cox1 sequences available at the time of this analysis, and one of those sequences was from a region other than the typical barcoding region (Folmer). Two of the sequences, Notocotylidae gen. sp. 1 NZ and sp. 2 NZ, were eventually removed from analyses because they did not align well. Therefore, the only sequences from GenBank left for phylogenetic comparisons with our sequences were Ogmocotyle sikae (mitochondrion, complete genome: NC_027112.1:6904–8460), Notocotylus sp. BOLD (KM538104), and Notocotylidae sp. MSB (KX670216).
3.1.1. The former Gorgoderidae
From BLAST results, several sequences in our dataset matched most closely to the sequence for Gorgoderina sp. (FJ477202) in GenBank. When attempting to find other sequences for use in downstream analyses, we found that nearly every species in this family was only represented by 28S or ITS. A cox1 sequence was available from Pseudophyllodistomum macrobranchiola (LC002523); however, the sequence was downstream of the Folmer region and did not overlap with our sequences. Upon further investigation, we found that these sequences matched very close to our other sequences for Notocotylidae sp., despite no BLAST matches from GenBank to Notocotylids. We therefore dissolved the Gorgoderidae sequence group, merging these sequences with the other Notocotylidae sequences, and have updated our previously published sequence (KT831348).
Our phylogenetic analyses have revealed four Notocotylid species from our samples. Both ML and BI trees agreed on topology with strong statistical support (Figure 2a). Though all ABGD methods agreed, they only split the groups into three (JC p max = 0.0215; K2 and simple p max = 0.0129): E. hortense, O. sikae, and Notocotylus sp. The only GenBank sequence to group with our sequences was Notocotylus sp. BOLD (KM538104).
Figure 2.
Molecular phylogeny of the Notocotylidae and Psilostomidae based on cox1. Bayesian inference phylogenies are given. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 are reported near the nodes, respectively. Accession numbers are given after species names. Emboldened taxa with three asterisks represent novel species from molecular analyses. (a) Notocotylidae. (b) Psilostomidae
Based on pairwise distances, however, Notocotylus sp. as a single group determined by ABGD was not supported based on the 5% cutoff, as several sequences within the group were more than 5% different from others, despite the average intraspecific divergence being 3.0% for all. Two sequences, isolates MGC683 and MGC1730, expressed 6.8%–10.2% and 5.0%–10.2% intraspecific divergence, respectively. Without including these sequences, the range of intraspecific divergence was 0.0%–5.6%, which is more reasonable for a single lineage, however, still beyond the cutoff. We suspected further division within the tree topology, as some sequences continued to be closer or above the 5% divergence cutoff. Those that grouped outside of the primary clade (identified as Notocotylus sp. A) and closer to MGC683 were then separated further and support by intraspecific divergence was then within the cutoff range. In doing this, the average interspecific divergence between Notocotylus sp. A and D is 3.8% with a range of 2.8%–5.6% (Appendix: Table A1).
In considering the snail host species, Notocotylus sp. B (MGC1730) and C (MGC683), utilized P. gyrina and H. trivolvis, respectively, clearly supporting differentiation. However, the other isolates within Notocotylus sp. A and D used both P. gyrina and S. elodes as hosts, but curiously, Notocotylus sp. A was a primary Physa infecting species (36 P. gyrina/three S. elodes), while Notocotylus sp. D was a primary Stagnicola infecting species (49 S. elodes/five P. gyrina).
3.2. Family Psilostomidae
Only a few species within the Psilostomidae had representation by cox1 in GenBank and significant overlap with our sequences. In molecular phylogenies, none of the sequences from this study grouped with any of the GenBank species representing the Psilostomidae family, but created their own monophyletic group, sister to P. varium. Both BI and ML trees agreed on topology (Figure 2b). The six sequences from this study were 0%–0.8% divergent from each other, with an average intraspecific divergence of 0.4%, and interspecific divergence of 14.3%–24.6% (Appendix: Table A2). Because of the low identity to any of the available genera from this family, the sequences from this study have therefore been identified broadly as Psilostomidae gen. sp. A. All six samples were derived from cercariae emerging from H. trivolvis snails.
3.3. Family Haematoloechidae
Despite there being 18 Haematoloechus spp. with cox1 sequences available in GenBank at the time, only two sequences from this database overlapped with our sequences because of different choices in sequenced cox1 regions. In addition, no other genera within the Haematoloechidae were currently represented in GenBank.
The four Haematoloechidae sequences from this study were 100% identical to each other, but 13.4%–25.8% divergent from GenBank sequences (Figure 3a and Appendix: Table A3). These four sequences were generalized to Haematoloechidae gen. sp. A, because there were no specific species within GenBank or other evidence that could provide more specificity at this time. Both BI and ML trees agreed with strong support for topology, as suspected for such little information. All four sequences were derived from samples that came from S. elodes snails collected at Pelican Point at Buffalo Lake.
Figure 3.
Molecular phylogeny of the Haematoloechidae and Plagiorchiidae based on cox1. Bayesian inference phylogenies are given. Clades representing a single species have been condensed for space. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 are reported near the nodes, respectively. Accession numbers are given after species names. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. Emboldened taxa with three asterisks represent novel species from molecular analyses. (a) Haematoloechidae. (b) Plagiorchiidae
3.4. Family Plagiorchiidae
Most Plagiorchiidae sequences in GenBank use a different region of the cox1 gene, downstream from the Folmer region. The only sequence that aligned with ours was one Plagiorchis sp. (FJ477214). Phylogenetic analyses of Plagiorchiid sequences resulted in both ML and BI trees agreeing on topology with strong statistical support for external nodes and moderate support for internal nodes (Figure 3b). All methods within ABGD supported the differentiation of lineages within the tree to nine groups other than the out‐group (p max (All) = 0.004–0.0599). Pairwise and averaged intraspecific divergence values were supported by the 5% cutoff, and the highest value was 2.1% within Lineage 1. The average interspecific divergence had a range from 8.9% to 18.8% (Appendix: Table A4). Further support for the differentiation of some lineages was found among intermediate host use, as Lineage 6 utilized H. trivolvis, Lineage 7 used L. stagnalis, and all other lineages were found emerging from S. elodes. Because this diversity was greater than we had expected by morphology (indicating possibly two species based on relative size) and prior BLAST results, we were unable to assign the unsequenced samples to these nine different lineages. Therefore, in downstream diversity analyses that require abundance information, these lineages have been conservatively lumped into one species, called Plagiorchis sp.
3.5. Family Echinostomatidae
For each separate alignment, ML and BI phylogenies were compared and found to agree on major topology. In instances where external node topology disagreed between the two methods, this was identified as a separate tree.
3.5.1. Drepanocephalus
Both nad1 sequences from this study grouped monophyletically with D. auritus sequences. Drepanocephalus sp. was paraphyletic to the D. auritus group and displayed a nucleotide divergence range to the D. auritus group of 14.4%–15.5% (Figure 4a). The intraspecific divergence within the auritus group ranged from 0.0% to 4.4%, with an average of 2.2% (Appendix: Table A5). Both samples from this study came from H. trivolvis snails, which match with other records of specimens derived from planorbid snails in different geographical regions, specifically the United States and Brazil (Table 3). Recent work has revealed the synonymy of D. auritus with Drepanocephalus spathans, with spathans as the chosen name (Hernández‐Cruz, Hernández‐Orts, Sereno‐Uribe, Pérez‐Ponce de León, & García‐Varela, 2016). Therefore, we have identified our sequences according to this.
Figure 4.
Molecular phylogeny of the Echinostomatidae: Drepanocephalus and Neopetasiger genera based on nad1. Bayesian inference phylogenies are given. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 from BI and ML analyses are reported near the nodes, respectively. Accession numbers are given after species names. Clades representing a single species have been condensed for space. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. (a) Drepanocephalus. (b) Neopetasiger
Table 3.
Host associations, geographical origins, and life stages of specimen sequences used in phylogenies
| Family | Species | Host | Host Type | Location | GenBank Accession Number(s) | Reference | |
|---|---|---|---|---|---|---|---|
| cox1 | nad1 | ||||||
| Diplostomidae | Alaria sp. 1 | Lithobates pipiens | 2 | Canada: Quebec, Saint Lawrence River | JF769439 | (Locke, McLaughlin, Lapierre, Johnson, & Marcogliese, 2011) | |
| Diplostomidae | Alaria sp. 2 | Pseudacris regilla, Anaxyrus boreas | 2 | USA: California, Bart's Pond; San Martin, Weed Pond | JF904535, JF904534, JF904536 | (Locke et al., 2011) | |
| Diplostomidae | Austrodiplostomum ostrowskiae | Biomphalaria obstructa, Dorosoma cepedianum | 1, 2 | USA: Noxubee County, MS;USA: Dallas County, AL | KT728795, KT728798, KT728799 | (Rosser et al., 2016) | |
| Diplostomidae | Austrodiplostomum sp. 1 | Pomoxis nigromaculatus | 2 | USA: Florida, Tampa, Lake Seminole | KR271029 | (Locke et al., 2015) | |
| Diplostomidae | Austrodiplostomum sp. 2 | Mugil cephalus | 2 | USA: Florida, Tampa, Lake Seminole | KR271032 | (Locke et al., 2015) | |
| Diplostomidae | Austrodiplostomum sp. 2 | Menidia beryllina, Ictalurus punctatus | 2 | USA: Mississippi | KU707943, KU707945 | (Rosser et al., 2016) | |
| Diplostomidae | Bolbophorus damnificus | Menidia beryllina | 2 | USA: Mississippi | KU707937 | (Rosser et al., 2016) | |
| Diplostomidae | Bolbophorus sp. | Pimephales promelas | 2 | Canada: Alberta, Coaldale, McQuillan Lake | KM538081 | (Van Steenkiste, Locke, Castelin, Marcogliese, & Abbott, 2014) | |
| Diplostomidae | Bolbophorus sp. | Menidia beryllina | 2 | USA: Mississippi | KU707938, KU707939 | (Rosser et al., 2016) | |
| Diplostomidae | Bolbophorus sp. | Helisoma trivolvis | 1 | Canada: Alberta, Buffalo Lake | KT831373 | (Gordy, Kish, Tarrabain, & Hanington, 2016) | |
| Diplostomidae | Bolbophorus sp. | Helisoma trivolvis | 1 | Canada: Alberta, Buffalo Lake, Isle Lake, Wabamun Lake | MH368843, MH368847, MH368850, MH368862, MH368871, MH368892, MH368918, MH368919 | Present study | |
| Diplostomidae | Crocodillicola pseudostoma (out) | Rhamdia guatemalensis | 2 | Mexico: Veracruz, Catemaco Lake | MF398317, MF398318 | (Hernández‐Mena, García‐Varela, & Pérez‐Ponce de León, 2017) | |
| Diplostomidae | Diplostomidae gen. sp. O *** | Physa gyrina | 1 | Canada: Alberta, Buffalo Lake | KT831363§ | (Gordy et al., 2016) | |
| Diplostomidae | Diplostomidae gen. sp. O*** | Physa gyrina | 1 | Canada: Alberta, Buffalo Lake, Wabamun Lake, Gull Lake, Isle Lake | MH368825, MH368851, MH368854, MH368855, MH368879, MH368880, MH368881, MH368882, MH368883, MH368884, MH368885, MH368886, MH368887, MH368888, MH368889, MH368890, MH368893, MH368903, MH368904, MH368905, MH368906, MH368915, MH368916, MH368917, MH368934, MH368935, MH368936, MH368937, MH368938, MH368939, MH368940, MH368941, MH368942 | Present study | |
| Diplostomidae | Diplostomidae gen. sp. X*** | Physa gyrina | 1 | Canada: Alberta, Isle Lake | MH368907 | Present study | |
| Diplostomidae | Diplostomum ardeae | Ardea herodias | 3 | Canada: Quebec, Montreal | KR271033 | (Locke et al., 2015) | |
| Diplostomidae | Diplostomum baeri LIN1 | Perca fluviatilis | 2 | Germany: Lake Constance | JQ639181, JQ639182 | (Behrmann‐Godel, 2013) | |
| Diplostomidae | Diplostomum baeri LIN2 | Not given | 3 | Canada: Quebec, Montreal | GQ292501 | (Locke, McLaughlin, Dayanandan, & Marcogliese, 2010) | |
| Diplostomidae | Diplostomum baeri LIN2 | Stagnicola elodes | 1 | Canada: Alberta, Wabamun Lake, Isle Lake | MH368863, MH368874, MH368875, MH368928 | Present study | |
| Diplostomidae | Diplostomum huronense | Notemigonus crysoleuca, Larus delawarensis | 2, 3 | Canada: Ontario | FJ477197 | (Moszczynska, Locke, McLaughlin, Marcogliese, & Crease, 2009) | |
| Diplostomidae | Diplostomum huronense | Perca flavescens, Notemigonus crysoleucas | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Louis, Beauharnois, Dorval Island | HM064671, HM064672 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum indistinctum | Catostomidae | 3 | Canada: Quebec | FJ477196 | (Moszczynska et al., 2009) | |
| Diplostomidae | Diplostomum indistinctum | Neogobius melanostomus | 2 | Canada: Quebec | GQ292482 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum indistinctum | Catostomus commersoni | 2 | Canada: Quebec, St. Lawrence River, Lake Saint | HM064673 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Diplostomum indistinctum | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake | KT831379 | (Gordy et al., 2016) | |
| Diplostomidae | Diplostomum mergi | Radix auricularia | 1 | Germany: Hengsteysee | KR149526, KR149527, KR149528 | (Selbach, Soldánová, Georgieva, Kostadinova, & Sures, 2015) | |
| Diplostomidae | Diplostomum parviventosum | Radix auricularia | 1 | Germany: Hengsteysee | KR149510, KR149511, KR149512 | (Selbach et al., 2015) | |
| Diplostomidae | Diplostomum pseudospathaceum | Stagnicola palustris | 1 | Germany: Hengsteysee | KR149544, KR149545, KR149546 | (Selbach et al., 2015) | |
| Diplostomidae | Diplostomum sp. 1 | Larus delawarensis | 3 | Canada: Quebec, Laurentides | GQ292479, GQ292480, GQ292481 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 1 | Stagnicola elodes | 1 | Canada: Alberta, Wabamun Lake, Isle Lake | MH368857, MH368896, MH368932, MH368943, MH368945 | Present study | |
| Diplostomidae | Diplostomum sp. 2 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River | GQ292486 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 3 | Micropterus salmoides | 2 | Canada: Quebec, St. Lawrence River | GQ292487 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 3 | Lymnaea stagnalis | 1 | Canada: Alberta, Wabamun Lake | KT831358 | (Gordy et al., 2016) | |
| Diplostomidae | Diplostomum sp. 3 | Lymnaea stagnalis | 1 | Canada: Alberta, Wabamun Lake | MH368837, MH368858 | Present study | |
| Diplostomidae | Diplostomum sp. 4 | Larus delawarensis | 3 | Canada: Quebec, Laurentides | GQ292494, GQ292495 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 4 | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | KT831354 | (Gordy et al., 2016) | |
| Diplostomidae | Diplostomum sp. 4 | Stagnicola elodes | 1 | Canada: Alberta, Wabamun Lake, Isle Lake, Gull Lake, Buffalo Lake, Lac La Nonne | MH368808, MH368809, MH368813, MH368814, MH368815, MH368816, MH368818, MH368819, MH368820, MH368821, MH368822, MH368823, MH368824, MH368826, MH368827, MH368828, MH368829, MH368830, MH368831, MH368832, MH368833, MH368834, MH368835, MH368836, MH368838, MH368839, MH368840, MH368841, MH368844, MH368845, MH368846, MH368848, MH368849, MH368853, MH368856, MH368859, MH368860, MH368861, MH368864, MH368865, MH368866, MH368867, MH368868, MH368869, MH368870, MH368872, MH368873, MH368876, MH368877, MH368891, MH368898, MH368899, MH368900, MH368901, MH368911, MH368913, MH368914, MH368924, MH368925, MH368926, MH368927, MH368929, MH368930, MH368931, MH368944, MH368946, MH368947, MH368948, MH368949, MH368950 | Present study | |
| Diplostomidae | Diplostomum sp. 6 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River | GQ292499 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 7 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River | GQ292500 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 8 | Rana pipiens | 2 | Canada: Quebec, Monteregie | GQ292497 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. 9 | Percina caprodes | 2 | Canada: Quebec, St. Lawrence River | GQ292496 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH368817 | Present study | |
| Diplostomidae | Diplostomum sp. B*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | MH368933 | Present study | |
| Diplostomidae | Diplostomum sp. C*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Wabamun Lake, Isle Lake | KT831360§, KT831378§, KT831382§ | (Gordy et al., 2016) | |
| Diplostomidae | Diplostomum sp. C*** | Stagnicola elodes, Helisoma trivolvis (MGC208) | 1 | Canada: Alberta, Gull Lake, Wabamun Lake, Isle Lake | MH368810, MH368811, MH368812, MH368852, MH368895, MH368902, MH368921, MH368922, MH368923 | Present study | |
| Diplostomidae | Diplostomum sp. clade Q | Radix auricularia | 1 | Germany: Hengsteysee | KR149554 | (Selbach et al., 2015) | |
| Diplostomidae | Diplostomum sp. LIN6 | Gasterosteus aculeatus | 2 | Norway: Troms, Takvatnet | KM212051, KM212052, KM212053 | (Kuhn et al., 2015) | |
| Diplostomidae | Diplostomum spathaceum | Acanthobrama marmid, Perca fluviatilis, Barbus luteus | 2 | Iraq: Saladin, Tikreet, Tigris River; Italy: Lecco, Lake Como, Oliveto Lario | KR271467, KR271468, KR271469 | (Locke, McLaughlin, Dayanandan, et al., 2010) | |
| Diplostomidae | Diplostomum spathaceum | unknown | unknown, likely China | KT736038 | Dang, R., et al., 2015, Unpublished | ||
| Diplostomidae | Hysteromorpha triloba | Catostomus, Notemigonus crysoleucas | 2 | Canada: Nova Scotia, Sackville, Feely Lake; Canada: Quebec, Outaouais, Ottawa River, Wendover | JF769475, JF769476 | (Locke et al., 2011) | |
| Diplostomidae | Neodiplostomum americanum | Lithobates aurora | 2 | USA: California, HMB 05 | JF904537, JF904538, JF769455 | (Locke et al., 2011) | |
| Diplostomidae | Neodiplostomum americanum | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | KT831357§ | (Gordy et al., 2016) | |
| Diplostomidae | Ornithodiplostomum scardinii | Scardinius erythrophthalmus | 2 | Czech Republic: Lake Macha | KX931425 | (Stoyanov et al., 2017) | |
| Diplostomidae | Ornithodiplostomum scardinii (out) | Scardinius erythrophthalmus | 2 | Czech Republic: Lake Macha | KX931425 | (Stoyanov et al., 2017) | |
| Diplostomidae | Ornithodiplostomum sp. 1 | Etheostoma nigrum | 2 | Canada: Ontario, St. Lawrence River | FJ477208 | (Moszczynska et al., 2009) | |
| Diplostomidae | Ornithodiplostomum sp. 1 | Etheostoma nigrum | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois, Pointe Dupuis (LSF‐2) | HM064742 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Ornithodiplostomum sp. 2 | Physa gyrina | 1 | Canada: Alberta, Wabamun Lake | KT831368 | (Gordy et al., 2016) | |
| Diplostomidae | Ornithodiplostomum sp. 2 | Notemigonus crysoleucas | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Louis, Beauharnois | HM064766, HM064768 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Ornithodiplostomum sp. 2 | Notemigonus crysoleucas | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Louis | FJ477210 | (Moszczynska et al., 2009) | |
| Diplostomidae | Ornithodiplostomum sp. 2 | Physa gyrina | 1 | Canada: Alberta, Wabamun Lake | KT831368 | (Gordy et al., 2016) | |
| Diplostomidae | Ornithodiplostomum sp. 3 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois, Pointe Dupuis (LSF‐2), Beauharnois | HM064782, HM064780 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Ornithodiplostomum sp. 3 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois, Pointe Dupuis (LSF‐2), Beauharnois | FJ477211 | (Moszczynska et al., 2009) | |
| Diplostomidae | Ornithodiplostomum sp. 4 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois, Pointe Dupuis (LSF‐2), Beauharnois | HM064786, HM064788 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Ornithodiplostomum sp. 4 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois, Pointe Dupuis (LSF‐2), Beauharnois | FJ477212 | (Moszczynska et al., 2009) | |
| Diplostomidae | Ornithodiplostomum sp. 8 | Pimephales notatus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Ile aux Ours | HM064789 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Ornithodiplostomum sp. 8 | Physa gyrina | 1 | Canada: Alberta, Pigeon Lake | KT831383 | (Gordy et al., 2016) | |
| Diplostomidae | Ornithodiplostomum sp. 8 | Physa gyrina | 1 | Canada: Alberta, Isle Lake | MH368908, MH368910, MH368920 | Present study | |
| Diplostomidae | Posthodiplostomum brevicaudatum | Perca fluviatilis, Gasterosteus aculeatus | 2 | Czech Republic: Lake Macha; Bulgaria: Lake Atanasovsko | KX931418, KX931419, KX931420 | (Stoyanov et al., 2017) | |
| Diplostomidae | Posthodiplostomum centrarchi | Lepomis gibbosus, Ardea cinerea | 2, 3 | Bulgaria: Lake Atanasovsko; Spain: Lagoon Bassa de les Olles, Ebro Delta; Slovakia: River Danube near Sturovo | KX931421, KX931422, KX931423 | (Stoyanov et al., 2017) | |
| Diplostomidae | Posthodiplostomum cuticola | Planorbis planorbis | 1 | Lithuania: Curonian Bay near Juodkrante | KX931424 | (Stoyanov et al., 2017) | |
| Diplostomidae | Posthodiplostomum sp. 1 | Ambloplites rupestris | 2 | Canada: Ontario, St. Lawrence River | FJ477215 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 2 | Lepomis gibbosus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Ile aux Ours | FJ477216 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 3* | Lepomis gibbosus | 2 | Canada: Quebec, St. Lawrence River, Beauharnois | FJ477217 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 4 | Lepomis gibbosus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Ile aux Ours | FJ477218 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 4 | Ardea herodias | 3 | Canada: Quebec, Lac Saint‐Pierre, Grand Ile | HM064844 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Posthodiplostomum sp. 4 | Physa gyrina | 1 | Canada: Alberta, Isle Lake | MH368909, MH368912 | Present study | |
| Diplostomidae | Posthodiplostomum sp. 5 | Lepomis gibbosus | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Iles aux Sables | FJ477219 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 7 | Perca flavescens | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Iles aux Sables | FJ477221 | (Moszczynska et al., 2009) | |
| Diplostomidae | Posthodiplostomum sp. 7 | Perca flavescens | 2 | Canada: Quebec, St. Lawrence River, Beauharnois | HM064865, HM064871 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Posthodiplostomum sp. 8 | Micropterus dolomieu | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Iles aux Sables | HM064873, HM064874, HM064875 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Tylodelphys aztecae | Skiffia lermae, Gila conspersa | 2 | Mexico | KT175367, KT175368, KT175369 | (García‐Varela, Sereno‐Uribe, Pinacho‐Pinacho, Domínguez‐Domínguez, & Pérez‐Ponce de León, 2016) | |
| Diplostomidae | Tylodelphys clavata | Perca fluviatilis | 2 | Germany: Lake Constance | JQ639201, JQ639202, JQ639203, JQ639204 | (Behrmann‐Godel, 2013) | |
| Diplostomidae | Tylodelphys clavata | Radix auricularia | 1 | Germany: Hengsteysee | JX986908 | (Georgieva, Soldánová, et al., 2013) | |
| Diplostomidae | Tylodelphys clavata | Perca fluviatilis | 2 | Romania: Danube Delta;Italy: Lombardy, Brescia, Oglio River;Italy: Lecco, Lake Como, Oliveto Lario | KR271478, KR271479, KR271480 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys excavata | Planorbarius corneus | 1 | Czech Republic: Pond Bohdanec | KC685344 | (Chibwana et al., 2013) | |
| Diplostomidae | Tylodelphys immer | Salvelinus fontinalis, Gavia immer | 2, 3 | Canada: Quebec, Bas‐Saint‐Laurent, Central, riviere Bic; Montreal | KR271491, KR271492, KR271493 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys jenynsiae | Cnesterodon decemmaculatus | 2 | Argentina: Buenos Aires, La Plata, Urban canal | KR271494, KR271495, KR271496 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys mashonensis | Clarias gariepinus | 2 | Tanzania: River Msimbazi, River Ruvu | KC685340, KC685341, KC685342, KC685343 | (Chibwana et al., 2013) | |
| Diplostomidae | Tylodelphys scheuringi | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Iles aux Sables | FJ477223 | (Moszczynska et al., 2009) | |
| Diplostomidae | Tylodelphys scheuringi | Perca flavescens, Ambloplites rupestris | 2 | Canada: Ontario, St. Lawrence River, Lake Saint Francois, LSF‐1; Lake Saint Louis, Dorval Island | HM064914, HM064915 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Diplostomidae | Tylodelphys scheuringi | Ambloplites rupestris, Perca flavescens | 2 | Canada: Ontario, St. Lawrence River, Pointe Dupuis (LSF‐2) | KR271508, KR271509 | (Chibwana et al., 2013) | |
| Diplostomidae | Tylodelphys sp. | Mystus tengara | 2 | India | KU725888, KU725889 | Chaudhary, A., et al., 2016, Unpublished | |
| Diplostomidae | Tylodelphys sp. | Gobiomorphus cotidianus | 2 | New Zealand | KU588147, KU588148, KU588149 | (Blasco‐Costa, Poulin, & Presswell, 2016) | |
| Diplostomidae | Tylodelphys sp. 2 LIN1 | Clarias gariepinus | 2 | Tanzania: Lake Victoria | KC685358 | (Chibwana et al., 2013) | |
| Diplostomidae | Tylodelphys sp. 2 LIN2 | Micropterus salmoides, Oreochromis leucostictus | 2 | Kenya: Rift Valley, Nakuru District, Lake Naivasha | KF809488, KF809494 | (Otachi, Locke, Jirsa, Fellner‐Frank, & Marcogliese, 2015) | |
| Diplostomidae | Tylodelphys sp. 3 | Lepomis microlophus | 2 | USA: Mississippi, Ascension Parish | KR271513, KR271514, KR271515 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys sp. 4 | Gobiomorus maculatus | 2 | Mexico: Oaxaca, Costa Chica, Playa Ventanilla, Laguna Ventanilla | KR271517, KR271518, KR271519 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys sp. 5 | Dormitator latifrons, Gobiomorus maculatus | 2 | Mexico: Oaxaca, Costa Chica, Playa Ventanilla, Laguna Ventanilla | KR271520, KR271521 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys sp. 6 | Poecilia latipinna | 2 | USA: Mississippi, Ascension Parish | KR271522, KR271523 | (Locke et al., 2015) | |
| Diplostomidae | Tylodelphys sp. A*** | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake | KT831356§ | (Gordy et al., 2016) | |
| Diplostomidae | Tylodelphys sp. A*** | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake | MH368842, MH368878, MH368894, MH368897 | Present study | |
| Echinostomatidae | Drepanocephalus auritus | Planorbella trivolvis, Biomphalaria straminea | 1 | USA; Brazil | KP053262, KP053263 | (Pinto, Griffin, Quiniou, Ware, & Melo, 2016) | |
| Echinostomatidae | Drepanocephalus auritus | Helisoma trivolvis | 1 | Canada: Alberta, Isle Lake, Buffalo Lake | MH368951, MH368952 | Present Study | |
| Echinostomatidae | Drepanocephalus auritus | Phalacrocorax auritus | 3 | Canada: Ontario, Lake Erie | KM538090 | (Van Steenkiste et al., 2014) | |
| Echinostomatidae | Drepanocephalus auritus | Phalacrocorax auritus | 3 | USA: lake Near Lakota, Nelson County, North Dakota; Lower Red Lake, Beltrami County, Minnesota; George County, Mississippi | KP683125, KP683126, KP683127, KP638128, KP683129, K638130, KP638131, KP638132 | (Kudlai, Kostadinova, Pulis, & Tkach, 2015) | |
| Echinostomatidae | Drepanocephalus auritus | Planorbella trivolvis | 1 | USA | KR259644 | (Pinto et al., 2016) | |
| Echinostomatidae | Drepanocephalus auritus | Helisoma trivolvis | 1 | Canada: Alberta, Buffalo Lake | KT831381 | (Gordy et al., 2016) | |
| Echinostomatidae | Drepanocephalus auritus | Helisoma trivolvis | 1 | Canada: Alberta, Buffalo Lake, Isle Lake | MH369294 | Present study | |
| Echinostomatidae | Drepanocephalus mexicanus | Phalacrocorax brasilianus | 3 | Mexico: Tobasco, Teapa | KY636228, KY636229 | (Hernández‐Cruz, Hernández‐Orts, Sereno‐Uribe, Pérez‐Ponce de León, & García‐Varela, 2018) | |
| Echinostomatidae | Drepanocephalus sp. | Biomphalaria straminea | 1 | Brazil | KP05264 | (Pinto et al., 2016) | |
| Echinostomatidae | Drepanocephalus spathans | Phalacrocorax brasilianus | 3 | Mexico: Durango, Rio Guatimape; Oaxaca, Presa Rio Verde | KY636233, KY636234 | (Hernández‐Cruz et al., 2018) | |
| Echinostomatidae | Echinoparyphium aconiatum | Lymnaea stagnalis | 1, 2 | Finland: Lake Pyykosjarvi | AY168946, AY168947 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Echinoparyphium ellisi | Anas platyrhynchos | 3 | New Zealand: Clutha River System, Central Otago District, South Island | KY436405, KY436406 | (Stoyanov et al., 2017) | |
| Echinostomatidae | Echinoparyphium poulini | Cygnus atratus | 3 | New Zealand: Pauerau, Central Otago District, South Island | KY436403, KY436404 | (Stoyanov et al., 2017) | |
| Echinostomatidae | Echinoparyphium recurvatum | Lymnaea peregra | 1 | UK: Wales, Lake Ceunant | AY168943, AY168944 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Echinoparyphium recurvatum | Pisidium casertanum, Sphaerium sp. | 2 | Norway: Lake Takvatn | KY513267, KY513269 | (Soldánová et al., 2017) | |
| Echinostomatidae | Echinoparyphium sp. 1A*** | Physa gyrina, Stagnicola elodes (MGC1954, MGC2104), Helisoma trivolvis (MGC2090) | 1 | Canada: Alberta, Lac La Nonne, Wabamun Lake, Isle Lake | MH368998, MH368999, MH369001, MH369002, MH369003, MH369004, MH369005, MH369006, MH369007, MH369008, MH369009, MH369010, MH369012, MH369013, MH369014, MH369015, MH369016, MH369017, MH369018, MH369019, MH369022, MH369023, MH369024, MH369025, MH369026, MH369028, MH369031, MH369032, MH369033, MH369034, MH369038, MH369042, MH369044, MH369045, MH369046, MH369047, MH369048, MH369049, MH369052, MH369053, MH369054, MH369055, MH369056, MH369059, MH369060, MH369062, MH369063, MH369065, MH369066, MH369068, MH369070, MH369075, MH369076, MH369087, MH369089, MH369090, MH369091, MH369093, MH369094, MH369095, MH369096, MH369097, MH369098, MH369099, MH369100, MH369101, MH369102, MH369121, MH369122, MH369123, MH369125, MH369131, MH369132, MH369133, MH369136, MH369147, MH369155, MH369156, MH369162, MH369163, MH369164, MH369165, MH369166, MH369167, MH369168, MH369178, MH369188, MH369191 | Present study | |
| Echinostomatidae | Echinoparyphium sp. 1A*** | Physa gyrina | 1 | Canada: Alberta, Lac La Nonne | KT831361§ | (Gordy et al., 2016) | |
| Echinostomatidae | Echinoparyphium sp. 1A*** | Physa gyrina, Stagnicola elodes (MGC1954, MGC2104), Helisoma trivolvis (MGC2090) | 1 | Canada: Alberta, Lac La Nonne, Wabamun Lake, Isle Lake | MH369243, MH369245, MH369246, MH369249, MH369250, MH369253, MH369255, MH369272, MH369273, MH369274, MH369277, MH369299, MH369300, MH369301, MH369302, MH369303, MH369304, MH369305 | Present study | |
| Echinostomatidae | Echinoparyphium sp. 1B*** | Physa gyrina | 1 | Canada: Alberta, Isle Lake | MH369181 | Present study | |
| Echinostomatidae | Echinoparyphium sp. A*** | Physa gyrina, Stagnicola elodes (MGC1932) | 1 | Canada: Alberta, Buffalo Lake, Wabamun Lake, Isle Lake, Lac La Nonne, Gull Lake, Pigeon Lake | MH369011, MH369035, MH369043, MH369051, MH369058, MH369061, MH369064, MH369069, MH369081, MH369082, MH369083, MH369084, MH369085, MH369113, MH369120, MH369128, MH369161, MH369169, MH369170, MH369171, MH369172, MH369173, MH369174, MH369175, MH369176, MH369177, MH369179, MH369180, MH369182, MH369183, MH369184, MH369185, MH369187, MH369190 | Present study | |
| Echinostomatidae | Echinoparyphium sp. A*** | Physa gyrina, Stagnicola elodes (MGC1932) | 1 | Canada: Alberta, Buffalo Lake, Wabamun Lake, Isle Lake, Lac La Nonne, Gull Lake, Pigeon Lake | MH369223, MH369247, MH369254, MH369257, MH369266, MH369289, MH369290, MH369291, MH369298, MH369306, MH369307, MH369308, MH369309, MH369310 | Present study | |
| Echinostomatidae | Echinoparyphium sp. A2*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne | MH369181 | Present study | |
| Echinostomatidae | Echinoparyphium sp. A2*** | Stagnicola elodes | 1 | Canada: Alberta, Lac La Nonne | KT831367§ | (Gordy et al., 2016) | |
| Echinostomatidae | Echinoparyphium sp. A2*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne | MH369232, MH369251, MH369258, MH369260, MH369265, MH369288 | Present study | |
| Echinostomatidae | Echinoparyphium sp. B*** | Stagnicola elodes | 1 | Canada: Alberta, Lac La Nonne | MH368969, MH368970, MH368971, MH368987, MH368988, MH369041, MH369074, MH369086, MH369092 | Present study | |
| Echinostomatidae | Echinoparyphium sp. C*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne | MH369088, MH369152 | Present study | |
| Echinostomatidae | Echinoparyphium sp. C*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne | MH369226, MH369228, MH369233, MH369234, MH369236, MH369237, MH369238, MH369239, MH369240, MH369241, MH369244, MH369252, MH369256, MH369259, MH369261, MH369262, MH369263, MH369264, MH369267, MH369278, MH369280, MH369282, MH369285, MH369296 | Present study | |
| Echinostomatidae | Echinoparyphium sp. D*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369189 | Present study | |
| Echinostomatidae | Echinoparyphium sp. E*** | Stagnicola elodes, Lymnaea stagnalis (MGC1878) | 1 | Canada: Alberta, Gull Lake | MH369109, MH369129, MH369134, MH369135, MH369159 | Present study | |
| Echinostomatidae | Echinoparyphium sp. E*** | Stagnicola elodes, Lymnaea stagnalis (MGC1878) | 1 | Canada: Alberta, Gull Lake | MH369275, MH369276 | Present study | |
| Echinostomatidae | Echinoparyphium sp. Lineage 1 | Ondatra zibethicus | 3 | USA: Wisconsin | GQ463103, GQ463104, GQ463105 | (Detwiler, Bos, & Minchella, 2010) | |
| Echinostomatidae | Echinoparyphium sp. Lineage 2 | Stagnicola elodes, Lymnaea stagnalis (MGC16A/B, MGC369), Helisoma trivolvis (MGC219) | 1 | Canada: Alberta, Gull Lake, Isle Lake, Buffalo Lake, Wabamun Lake, Lac La Nonne | MH368953, MH368954, MH368955, MH368956, MH368957, MH368959, MH368960, MH368961, MH368962, MH368963, MH368964, MH368965, MH368966, MH368967, MH368968, MH368972, MH368973, MH368974, MH368975, MH368976, MH368977, MH368978, MH368979, MH368980, MH368981, MH368982, MH368983, MH368984, MH368985, MH368986, MH368989, MH368990, MH368991, MH368992, MH368993, MH368994, MH368995, MH368996, MH368997, MH369000, MH369021, MH369027, MH369029, MH369036, MH369037, MH369039, MH369050, MH369057, MH369067, MH369071, MH369072, MH369073, MH369077, MH369078, MH369079, MH369103, MH369104, MH369105, MH369106, MH369107, MH369111, MH369112, MH369114, MH369115, MH369116, MH369117, MH369118, MH369119, MH369124, MH369126, MH369137, MH369138, MH369139, MH369140, MH369141, MH369142, MH369143, MH369144, MH369146, MH369148, MH369149, MH369150, MH369151, MH369153, MH369154, MH369160, MH369186 | Present study | |
| Echinostomatidae | Echinoparyphium sp. Lineage 2 | Lymnaea elodes | 1 | USA: Indiana, Pond A | GQ463119, GQ463120, GQ463121 | (Detwiler et al., 2010) | |
| Echinostomatidae | Echinoparyphium sp. Lineage 2 | Stagnicola elodes, Lymnaea stagnalis (MGC16A/B, MGC369), Helisoma trivolvis (MGC219) | 1 | Canada: Alberta, Gull Lake, Isle Lake, Buffalo Lake, Wabamun Lake, Lac La Nonne | MH369224, MH369225, MH369283, MH369293 | Present study | |
| Echinostomatidae | Echinoparyphium sp. Lineage 2 | Stagnicola elodes | 1 | Canada: Alberta, Lac La Nonne | KT831350§ | (Gordy et al., 2016) | |
| Echinostomatidae | Echinoparyphium sp. Lineage 3 | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake, Buffalo Lake | MH369130, MH369158 | Present study | |
| Echinostomatidae | Echinoparyphium sp. Lineage 3 | Helisoma trivolvis | 1, 2 | USA: Indiana, Pond A | GQ463122, GQ463123 | (Detwiler et al., 2010) | |
| Echinostomatidae | Echinoparyphium sp. Lineage 3 | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake, Buffalo Lake | MH369270 | Present study | |
| Echinostomatidae | Echinostoma bolschewense | Viviparus acerosus | 1 | Slovakia: Danube at Gabcikovo | KP065608, KP065621 | (Georgieva et al., 2014) | |
| Echinostomatidae | Echinostoma caproni | unknown | Madagascar; Egypt; Cameroon | AF025837, AF025838 | (Morgan & Blair, 1998) | ||
| Echinostomatidae | Echinostoma cf. friedi | Planorbis sp. | 1 | UK: Wales, Pwll Penarth | AY168937 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Echinostoma deserticum | unknown | Nigeria: Niger | AF025836 | (Morgan & Blair, 1998) | ||
| Echinostomatidae | Echinostoma hortense (out) | Dog | 3 | China | KR062182 | (Liu et al., 2016) | |
| Echinostomatidae | Echinostoma miyagawai | Anas platyrhynchos | 3 | New Zealand: Clutha River System, Central Otago District, South Island | KY436400 | (Stoyanov et al., 2017) | |
| Echinostomatidae | Echinostoma miyagawai | Planorbis planorbis, Aythya fuligula | 1, 3 | Czech Republic: Pond Louzek; vicinities of Tovacov | KP065632, KP065640 | (Georgieva et al., 2014) | |
| Echinostomatidae | Echinostoma nasincovae | Planorbarius corneus | 1 | Slovakia: Danube at Gabcikovo; Czech Republic: Pond Hluboky u Hamru | KP065659, KP065674 | (Georgieva et al., 2014) | |
| Echinostomatidae | Echinostoma novazealandense | Anas platyrhynchos | 3 | New Zealand: Clutha River System, Central Otago District, South Island | KY436398, KY436399 | (Stoyanov et al., 2017) | |
| Echinostomatidae | Echinostoma paraensei | Glyptophysa | 1 | Brazil; Australia: North Queensland, Townsville | AF025834, AF026282 | (Morgan & Blair, 1998) | |
| Echinostomatidae | Echinostoma paraulum | Lymnaea stagnalis, Aythya fuligula | 1, 3 | Germany: pond near Poppenwind; Czech Republic: vicinities of Tovacov | KP065677, KP065680 | (Georgieva et al., 2014) | |
| Echinostomatidae | Echinostoma revolutum Lineage A | Lymnaea peregra | 1 | Bulgaria: Grigorevo | AY168934 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Echinostoma revolutum Lineage A | Lymnaea stagnalis, Aythya fuligula | 1, 3 | Czech Republic: Pond Vlkovsky; vicinities of Tovacov; Pond Hluboky u Hamru | KP065646, KP065653, KP065658 | (Georgieva et al., 2014) | |
| Echinostomatidae | Echinostoma revolutum Lineage A | Domestic duck | 3 | Thailand | KP455631, KP455632, KP455633 | (Nagataki et al., 2015) | |
| Echinostomatidae | Echinostoma revolutum Lineage A | Columba livia f. domestica | 3 | Poland | KT726380 | Ledwon, A., et al., 2015, Unpublished | |
| Echinostomatidae | Echinostoma revolutum Lineage B | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake, Gull Lake, Wabamun Lake, Isle Lake, Lac La Nonne | MH369192, MH369193, MH369194, MH369195, MH369196, MH369197, MH369200, MH369201, MH369202, MH369204, MH369206, MH369207, MH369208, MH369209, MH369210, MH369211, MH369213, MH369214, MH369215, MH369216, MH369217, MH369218, MH369219, MH369220, MH369221, MH369222 | Present study | |
| Echinostomatidae | Echinostoma revolutum Lineage B | Lymnaea elodes | 1 | USA: Indiana, Pond A | GQ463056, GQ463057 | (Detwiler et al., 2010) | |
| Echinostomatidae | Echinostoma revolutum Lineage B | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake, Gull Lake, Wabamun Lake, Isle Lake, Lac La Nonne | MH369227, MH369229, MH369230, MH369231, MH369235, MH369242, MH369248, MH369268, MH369279, MH369281, MH369284, MH369286, MH369287, MH369292 | Present study | |
| Echinostomatidae | Echinostoma robustum | Lymnaea elodes, Biomphalaria glabrata, Gallus gallus | 1, 1, 3 | USA: Indiana, Pond A; Minnesota; Brazil | GQ463053*, GQ463054, GQ463055 | (Detwiler et al., 2010) | |
| Echinostomatidae | Echinostoma sp. | Hydromys chrysogaster | 3 | Australia: North Queensland, Townsville | AF026290 | (Morgan & Blair, 1998) | |
| Echinostomatidae | Echinostoma sp. IG | Radix auricularia | 1 | Germany: Hengsteysee | KC618449, KC618450 | (Georgieva, Selbach, et al., 2013) | |
| Echinostomatidae | Echinostoma sp. NZ‐Ad* | Branta canadensis | 3 | New Zealand | AF026289* | (Morgan & Blair, 1998) | |
| Echinostomatidae | Echinostoma trivolvis | Ondatra zibethicus | 3 | Canada: Ontario, Lake Opinicon | KM538091 | (Van Steenkiste et al., 2014) | |
| Echinostomatidae | Echinostoma trivolvis Lineage A | Helisoma trivolvis | 1 | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne | MH369198, MH369199, MH369203, MH369205, MH369212 | Present study | |
| Echinostomatidae | Echinostoma trivolvis Lineage A | Helisoma trivolvis | 1 | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne | MH369271 | Present study | |
| Echinostomatidae | Echinostoma trivolvis Lineage B | Ondatra zibethicus, Lymnaea elodes | 3, 1 | USA: Wisconsin; Minnesota | GQ463051, GQ463052, GQ463113 | (Detwiler et al., 2010) | |
| Echinostomatidae | Echinostoma trivolvis Lineage B | Ondontra zibethicus | 3 | USA: Virginia | JQ670857, JQ670859, JQ670850 | (Detwiler, Zajac, Minchella, & Belden, 2012) | |
| Echinostomatidae | Echinostoma trivolvis Lineage B | unknown | North America | AF025831 | (Morgan & Blair, 1998) | ||
| Echinostomatidae | Echinostomatidae gen. sp.*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369269, MH369295, MH369297 | Present study | |
| Echinostomatidae | Euparyphium capitaneum (out) | Anhinga anhinga | 3 | Mexico: Veracruz, Tecolutla; Nayarit, La Tovara | KY636235, KY636236 | (Hernández‐Cruz et al., 2018) | |
| Echinostomatidae | Fasciola hepatica (out) | Cattle | 3 | Iran | KT893744 | Akhlaghi, E., et al., 2015, Unpublished | |
| Echinostomatidae | Hypoderaeum conoideum | Lymnaea peregra | 1 | Bulgaria: Grigorevo | AY168949 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Hypoderaeum conoideum | Anas discors | 3 | Canada: Manitoba, Lake Manitoba, South shore, Delta Marsh | KM538101 | (Van Steenkiste et al., 2014) | |
| Echinostomatidae | Hypoderaeum sp. Lineage 1 | Lymnaea elodes | 1 | USA: Indiana, Pond A | GQ463100, GQ463101, GQ463102 | (Detwiler et al., 2010) | |
| Echinostomatidae | Hypoderaeum sp. Lineage 1 | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne, Wabamun Lake, Isle Lake | MH368958, MH369020, MH369030, MH369040, MH369080, MH369108, MH369110, MH369145, MH369157 | Present study | |
| Echinostomatidae | Isthmiophora melis (out) | Planorbis sp. | 1 | UK: Wales, Llyn Mawr | AY168948 | (Kostadinova & Herniou, 2003) | |
| Echinostomatidae | Neopetasiger islandicus | Planorbula armigera | 1 | Canada: Alberta, Wabamun Lake | KT831342 | (Gordy et al., 2016) | |
| Echinostomatidae | Neopetasiger neocomense | Podiceps cristatus | 3 | Czech Republic | JQ425591 | (Georgieva, Kostadinova, & Skirnisson, 2012) | |
| Echinostomatidae | Neopetasiger sp. 1 | Gyraulus albus | 1 | Germany: Lake Hennetalsperre | KM191808, KM191809 | (Selbach et al., 2014) | |
| Echinostomatidae | Neopetasiger sp. 2 | Gyraulus albus | 1 | Germany: Lake Hennetalsperre | KM191810, KM191811 | (Selbach et al., 2014) | |
| Echinostomatidae | Neopetasiger sp. 3 | Planorbis planorbis, Gyraulus albus | 1 | Germany: Lake Kleiner Ploener See; Lake Hennetalsperre | KM191814, KM191815, KM191816 | (Selbach et al., 2014) | |
| Echinostomatidae | Neopetasiger sp. 4 | Gasterosteus aculeatus | 2 | Canada: Lake Gosling | KM191817 | (Selbach et al., 2014) | |
| Echinostomatidae | Neopetasiger sp. 4 | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake | KT831343, KT831345 | (Gordy et al., 2016) | |
| Echinostomatidae | Neopetasiger sp. 4 | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake, Isle Lake, Buffalo Lake | MH369311, MH369312, MH369313, MH369314, MH369315, MH369316, MH369317, MH369318 | Present study | |
| Haematoloechidae | Haematoloechidae gen. sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | KT831372§ | (Gordy et al., 2016) | |
| Haematoloechidae | Haematoloechidae gen. sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369319, MH369320, MH369321 | Present study | |
| Haematoloechidae | Haematoloechus sp. | Rana pipiens | 3 | Canada: Quebec, Outaouais, Ottawa River, Wendover; Ontario, Southern Ontario, Chatham‐Kent, East of Lake St.Clair and St. Clair National Wildlife Area | KM538096, KM538097 | (Van Steenkiste et al., 2014) | |
| Notocotylidae | Notocotylidae gen. sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake | KT831348§, KT831364 | (Gordy et al., 2016) | |
| Notocotylidae | Notocotylidae gen. sp. A*** | Physa gyrina, Stagnicola elodes | 1 | Canada: Alberta, Wabamun Lake, Isle Lake, Gull Lake, Buffalo Lake, Lac La Nonne | MH369323, MH369405, MH369324, MH369406, MH369325, MH369326, MH369327, MH369407, MH369408, MH369328, MH369409, MH369329, MH369330, MH369331, MH369332, MH369333, MH369334, MH369335, MH369336, MH369337, MH369338, MH369339, MH369340, MH369341, MH369342, MH369343, MH369344, MH369345, MH369410, MH369346, MH369347, MH369348, MH369349, MH369350, MH369351, MH369352, MH369411, MH369353, MH369354, MH369355, MH369356, MH369357, MH369358, MH369359, MH369360, MH369361, MH369362, MH369363, MH369364, MH369365, MH369366, MH369367, MH369368, MH369412, MH369369, MH369370, MH369371, MH369372, MH369373, MH369374, MH369375, MH369376, MH369378, MH369413, MH369414, MH369379, MH369380, MH369381, MH369382, MH369383, MH369415, MH369416, MH369384, MH369385, MH369386, MH369387, MH369388, MH369389, MH369390, MH369391, MH369417, MH369392, MH369393, MH369394, MH369395, MH369396, MH369397, MH369398, MH369399, MH369400, MH369401, MH369402, MH369403, MH369404 | Present study | |
| Notocotylidae | Notocotylus sp. | Mergus merganser | 3 | Canada: Quebec, Hudson, Le Nichoir | KM538104 | (Van Steenkiste et al., 2014) | |
| Notocotylidae | Ogmocotyle sikae | Unknown | China: Hunan Province, Jishou City | KR006934(NC_027112:6904‐8460) | Ma, J., et al., 2015, Unpublished | ||
| Plagorchiidae | Plagiorchis sp. Lineage 1 | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne, Buffalo Lake | MH369420, MH369421, MH369422, MH369433, MH369434, MH369435, MH369441, MH369460, MH369461, MH369463, MH369464 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 2 | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369467 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 3 | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369442, MH369454, MH369466 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 4 | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne, Buffalo Lake, Wabamun Lake, Isle Lake | MH369418, MH369423, MH369425, MH369428, MH369429, MH369431, MH369432, MH369436, MH369437, MH369440, MH369447, MH369452, MH369453, MH369456, MH369462, MH369471 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 5 | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake, Lac La Nonne | MH369419, MH369426, MH369427 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 6 | Helisoma trivolvis | 1 | Canada: Alberta, Buffalo Lake | MH369470 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 7 | Lymnaea stagnalis | 1 | Canada: Alberta, Buffalo Lake, Gull Lake | MH369438, MH369448, MH369455, MH369458, MH369468, MH369469 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 8 | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake, Gull Lake | MH369449, MH369450, MH369451, MH369459, MH369465 | Present study | |
| Plagorchiidae | Plagiorchis sp. Lineage 9 | Stagnicola elodes | 1 | Canada: Alberta, Lac La Nonne, Buffalo Lake | MH369424, MH369430, MH369439, MH369443, MH369444, MH369445, MH369446 | Present study | |
| Plagorchiidae | Plagiorchis sp. | Larus delawarensis | 3 | Canada: Quebec, St. Lawrence River | FJ477214 | (Moszczynska et al., 2009) | |
| Psilostomidae | Echinochasmus japonicus (out) | Homo sapiens | 3 | Viet Nam: Phu Tho | NC_030518 | Le, T.H., et al., 2015, Unpublished | |
| Psilostomidae | Pseudopsilostoma varium | Phalacrocorax auritus | 3 | USA: Mississippi | JX468064 | (O'Hear et al., 2014) | |
| Psilostomidae | Psilostomatidae gen. sp. A*** | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake | MH369477§ | (Gordy et al., 2016) | |
| Psilostomidae | Psilostomatidae gen. sp. A*** | Helisoma trivolvis | 1 | Canada: Alberta, Wabamun Lake, Isle Lake | MH369473, MH369472, MH369476, MH369474, MH369475 | Present study | |
| Psilostomidae | Sphaeridiotrema globulus | Duck experimentally infected with metacercariae from Elimia virginica | 2, 3 | USA: Lake Musconetcong, New Jersey | GQ890329 | (Bergmame et al., 2011) | |
| Psilostomidae | Sphaeridiotrema pseudoglobulus | Duck experimentally infected with metacercariae from Bithynia tentaculata | 2, 3 | Canada: Riviere du Sud, Quebec | GQ890328 | (Bergmame et al., 2011) | |
| Psilostomidae | Sphaeridiotrema pseudoglobulus | Aythya affinis | 3 | Canada: Quebec, St. Lawrence River | FJ477222 | (Moszczynska et al., 2009) | |
| Strigeidae | Apatemon sp. 1 | Etheostoma nigrum | 2 | Canada: Quebec, St. Lawrence River, Lake St. Louis | FJ477183 | (Moszczynska et al., 2009) | |
| Strigeidae | Apatemon sp. 1 | Etheostoma nigrum | 2 | Canada: Ontario, St. Lawrence River, Lake Saint Francois | HM064633 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Apatemon sp. 1x | Etheostoma nigrum | 2 | Canada: Ontario, St. Lawrence River, Lake Saint Francois | HM064635, HM064636 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Apatemon sp. 3 | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake St. Pierre, Iles aux Sables | FJ477185 | (Moszczynska et al., 2009) | |
| Strigeidae | Apatemon sp. 3 | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake St. Pierre, Iles aux Sables | HM064645 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Apatemon sp. 4 | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Francois | FJ477186 | (Moszczynska et al., 2009) | |
| Strigeidae | Apatemon sp. 4 | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake St. Pierre, Iles aux Sables | HM064647 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Apatemon sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | MH369603, MH369604, MH369605, MH369606, MH369607, MH369608, MH369609, MH369610, MH369611, MH369612, MH369613, MH369614, MH369615, MH369616, MH369617 | Present study | |
| Strigeidae | Apatemon sp. B*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | MH369618 | Present study | |
| Strigeidae | Apatemon sp. C*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | MH369619, MH369620, MH369621, MH369622 | Present study | |
| Strigeidae | Apatemon sp. ‘jamiesoni’ | Potamopyrgus antipodarum, Gobiomorphus cotidianus | 1, 2 | New Zealand | KT334181, KT334182 | (Blasco‐Costa et al., 2016) | |
| Strigeidae | Apharyngostrigea pipientis (out) | Lithobates pipiens | 2 | Canada: Quebec, Monteregie, Boucherville, Etang Saulaie | HM064884, HM064885 | (Locke et al., 2011) | |
| Strigeidae | Apharynogstrigea cornu | Ardea alba | 3 | Mexico: Veracruz, Panuco | JX977777 | (Hernández‐Mena, García‐Prieto, & García‐Varela, 2014) | |
| Strigeidae | Apharynogstrigea cornu | Ardea herodias | 3 | Canada: Quebec, St. Lawrence River, Lake St. Louis, Ile aux Herons | JF769451 | (Locke et al., 2011) | |
| Strigeidae | Australapatemon burti LIN1 | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | KT831346, KT831351 | (Gordy et al., 2016) | |
| Strigeidae | Australapatemon burti LIN1 | Stagnicola elodes, Physa gyrina, Helisoma trivolvis, Helisoma campanulatum, Planorbis sp., Lymnaea stagnalis | 1 | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne, Gull Lake, Buffalo Lake | KY207548, KY207549, KY207551, KY207552, KY207553, KY207554, KY207555, KY207556, KY207559, KY207560, KY207561, KY207562, KY207563, KY207564, KY207565, KY207566, KY207567, KY207568, KY207570, KY207571, KY207572, KY207573, KY207574, KY207575, KY207576, KY207578, KY207579, KY207580, KY207581, KY207584, KY207585, KY207586, KY207588, KY207589, KY207590, KY207591, KY207592, KY207593, KY207594, KY207595, KY207598, KY207599, KY207600, KY207601, KY207602, KY207603, KY207604, KY207605, KY207606, KY207607, KY207608, KY207609, KY207610, KY207611, KY207612, KY207614, KY207617, KY207618, KY207619, KY207620, KY207621, KY207623, KY207624, KY587399, KY587398, KY587394, KY587401, HM385485, KY587400, HM385486 | (Gordy, Locke, Rawlings, Lapierre, & Hanington, 2017) | |
| Strigeidae | Australapatemon burti LIN1 | Stagnicola elodes, Physa gyrina, Helisoma trivolvis | 1 | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne, Gull Lake, Buffalo Lake | MH369623, MH369624, MH369625, MH369626, MH369627, MH369628, MH369629, MH369630, MH369631, MH369632, MH369633, MH369634, MH369635, MH369636, MH369637, MH369638, MH369639, MH369640, MH369641, MH369642, MH369643, MH369644, MH369645, MH369646, MH369647, MH369648, MH369649, MH369650, MH369651, MH369652, MH369653, MH369654, MH369655, MH369656, MH369657, MH369658, MH369659, MH369660, MH369661, MH369662, MH369663, MH369664, MH369665, MH369666, MH369667, MH369668, MH369669, MH369670, MH369671, MH369672, MH369673, MH369674, MH369675, MH369676, MH369677, MH369678, MH369679, MH369680, MH369681, MH369682, MH369683, MH369684, MH369686, MH369687, MH369688, MH369689, MH369690, MH369691, MH369692, MH369693, MH369694, MH369695, MH369696, MH369697, MH369698, MH369699, MH369700, MH369701, MH369702, MH369703, MH369704, MH369705, MH369706, MH369707, MH369708, MH369709, MH369710, MH369711, MH369712, MH369713, MH369714, MH369715, MH369716, MH369717, MH369718, MH369719, MH369720, MH369721, MH369722, MH369723, MH369724, MH369725, MH369726, MH369727, MH369728, MH369729, MH369730, MH369731, MH369732, MH369733, MH369734, MH369735, MH369736, MH369737, MH369738, MH369739, MH369740, MH369741, MH369742, MH369743, MH369744, MH369745, MH369746, MH369747, MH369748, MH369749, MH369750, MH369751, MH369752, MH369753, MH369754, MH369755, MH369756, MH369757, MH369758, MH369759, MH369760, MH369761, MH369762, MH369763, MH369685 | Present study | |
| Strigeidae | Australapatemon mclaughlini | Anas americana | 3 | Mexico: Baja California Sur, Guerrero Negro | JX977725 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Australapatemon mclaughlini | Physa gyrina, Anas acuta | 1, 3 | Canada: Alberta, Buffalo Lake; Ontario | KY207615, KY207627, KY207628 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon mclaughlini | Physa gyrina | 1 | Canada: Alberta, Buffalo Lake | MH369764 | Present study | |
| Strigeidae | Australapatemon niewiadomski | Barbronia weberi, Anas platyrhynchos | 2, 3 | New Zealand | KT334176, KT334177, KT334178, KT334179, KT334180 | (Blasco‐Costa et al., 2016) | |
| Strigeidae | Australapatemon sp. LIN2 | Bucephala albeola | 3 | Canada: Ontario | HM385535 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN3 | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake | KY207577 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN4 | Physa gyrina, Aythya collaris | 1, 3 | Canada: Alberta, Lac La Nonne; Ontario | KY207569, KY587397, KY587396 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN4 | Physa gyrina | 1 | Canada: Alberta, Gull Lake | MH369765 | Present study | |
| Strigeidae | Australapatemon sp. LIN5 | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | KY207597 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN6 | Anas cyanoptera | 3 | Mexico: Estado de Mexico | JX977726 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Australapatemon sp. LIN6 | Physa gyrina | 1 | Canada: Alberta, Pigeon Lake, Isle Lake | KY207613, KY207616 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN6 | Physa gyrina | 1 | Canada: Alberta, Isle Lake, Buffalo Lake, Lac La Nonne | MH369766, MH369767, MH369768, MH369769, MH369770 | Present study | |
| Strigeidae | Australapatemon sp. LIN8 | Oxyura jamaicensis | 3 | Mexico: Durango, Guatimape | JX977728 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Australapatemon sp. LIN8 | Physa gyrina, Oxyura jamaicensis | 1, 3 | Canada: Alberta, Isle Lake, Buffalo Lake; Ontario | KY207587, KY207622, HM385538, HM385537, HM385536 | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN8 | Physa gyrina | 1 | Canada: Alberta, Isle Lake, Buffalo Lake, Gull Lake | MH369771, MH369772, MH369773, MH369774, MH369775, MH369776, MH369777 | Present study | |
| Strigeidae | Australapatemon sp. LIN9A | Stagnicola elodes, Anas acuta | 1, 3 | Canada: Alberta, Gull Lake, Isle Lake, Buffalo Lake; Ontario | KY207550§, KY207557§, KY207558§, KY207582§, KY207596§, HM385534§ | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN9A | Stagnicola elodes, Lymnaea stagnalis (MGC176B) | 1 | Canada: Alberta, Lac La None, Gull Lake, Buffalo Lake, Isle Lake | MH369779, MH369780, MH369781, MH369782, MH369783, MH369784, MH369785, MH369786, MH369787, MH369788, MH369789, MH369778 | Present study | |
| Strigeidae | Australapatemon sp. LIN9B | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | KY207583§ | (Gordy et al., 2017) | |
| Strigeidae | Australapatemon sp. LIN9B | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake | MH369790, MH369791, MH369792 | Present study | |
| Strigeidae | Australapatemon sp. LIN10*** | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake | MH369793 | Present study | |
| Strigeidae | Cardiocephaloides medioconiger | Larus sp. | 3 | Mexico: Laguna de Términos, Campeche | JX977782, JX977783 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Cardiocephaloides sp. | Larus occidentalis | 3 | Mexico: Baja California Sur, Guerrero Negro | JX977784 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Cotylurus cornutus | Radix balthica, Gyraulus acronicus | 1 | Norway: Lake Takvatn | KY513231, KY513232, KY513233, KY513234, KY513235, KY513236 | (Soldánová et al., 2017) | |
| Strigeidae | Cotylurus cornutus | Stagnicola elodes | 1 | Canada: Alberta, Gull Lake | KT831347§ | (Gordy et al., 2017) | |
| Strigeidae | Cotylurus cornutus | Stagnicola elodes, Helisoma trivolvis (MGC205) | 1 | Canada: Alberta, Gull Lake, Isle Lake, Lac La Nonne | MH369478, MH369480, MH369484, MH369485, MH369486, MH369487, MH369488, MH369489, MH369490, MH369491, MH369492, MH369493, MH369494, MH369495, MH369496, MH369497, MH369498, MH369500, MH369501, MH369502, MH369503, MH369504, MH369505, MH369509, MH369510, MH369511, MH369516, MH369532, MH369538, MH369539, MH369544, MH369557, MH369597, MH369601 | Present study | |
| Strigeidae | Cotylurus gallinulae | Aythya affinis | 3 | Mexico: Sonora, La esperanza | JX977781 | (Hernández‐Mena et al., 2014) | |
| Strigeidae | Cotylurus gallinulae | Physa gyrina | 1 | Canada: Alberta, Buffalo Lake, Wabamun Lake, Isle Lake, Lac La Nonne | MH369517, MH369518, MH369525, MH369526, MH369527, MH369528, MH369529, MH369560, MH369571, MH369572, MH369574, MH369575, MH369577, MH369583, MH369584, MH369587, MH369588, MH369590, MH369595, MH369596, MH369599, MH369600 | Present study | |
| Strigeidae | Cotylurus sp. A*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | KT831371§ | (Gordy et al., 2016) | |
| Strigeidae | Cotylurus sp. A*** | Stagnicola elodes, Physa gyrina (MGC1962) | 1 | Canada: Alberta, Isle Lake, Lac La Nonne, Wabamun | MH369513, MH369520, MH369521, MH369522, MH369523, MH369524, MH369533, MH369537, MH369541, MH369542, MH369543, MH369545, MH369546, MH369547, MH369548, MH369549, MH369550, MH369551, MH369552, MH369554, MH369555, MH369556, MH369558, MH369559, MH369561, MH369562, MH369573, MH369578, MH369579, MH369580, MH369581, MH369582, MH369585, MH369589, MH369591, MH369594, MH369598, MH369602 | Present study | |
| Strigeidae | Cotylurus sp. B*** | Physa gyrina | 1 | Canada: Alberta, Isle Lake | MH369586 | Present study | |
| Strigeidae | Cotylurus sp. C*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake, Gull Lake, Isle Lake, Lac La Nonne | MH369479, MH369481, MH369515, MH369530, MH369531, MH369553, MH369564 | Present study | |
| Strigeidae | Cotylurus sp. D*** | Stagnicola elodes | 1 | Canada: Alberta, Buffalo Lake, Gull Lake, Isle Lake, Lac La Nonne | MH369482, MH369483, MH369499, MH369506, MH369507, MH369508, MH369534, MH369535, MH369536, MH369540, MH369565, MH369593 | Present study | |
| Strigeidae | Cotylurus sp. E*** | Lymnaea stagnalis | 1 | Canada: Alberta, Buffalo Lake, Wabamun Lake | MH369512, MH369514, MH369567, MH369568, MH369569, MH369570 | Present study | |
| Strigeidae | Cotylurus sp. F*** | Stagnicola elodes | 1 | Canada: Alberta, Isle Lake | MH369519 | Present study | |
| Strigeidae | Cotylurus sp. G*** | Lymnaea stagnalis | 1 | Canada: Alberta, Buffalo Lake | MH369563, MH369566, MH369576 | Present study | |
| Strigeidae | Cotylurus sp. H*** | Physa gyrina | 1 | Canada: Alberta, Buffalo Lake | MH369592 | Present study | |
| Strigeidae | Ichthyocotylurus pileatus | Perca flavescens, Etheostoma nigrum | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Louis, Beauharnois | HM064721, HM064726 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Ichthyocotylurus pileatus | Perca flavescens | 2 | Canada: Ontario, St. Lawrence River, Lake Saint Francois | FJ477204 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Ichthyocotylurus sp. 2 | Perca flavescens | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Louis, Beauharnois | HM064728 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Ichthyocotylurus sp. 3 | Notropis hudsonius | 2 | Canada: Ontario, St. Lawrence River, Lake Saint Francois | HM064729 | (Locke, McLaughlin, & Marcogliese, 2010) | |
| Strigeidae | Tylodelphys scheuringi (out) | Ambloplites rupestris | 2 | Canada: Quebec, St. Lawrence River, Lake Saint Pierre, Iles aux Sables | FJ477223 | (Moszczynska et al., 2009) | |
Novel by molecular phylogeny; § Record updated in present study; Host Type: 1= First Intermediate, 2 = Second Intermediate, 3 = Definitive
Most likely Posthodiplostomum centrarchi
Rows highlighted in gray represent sequences from the present study
3.5.2. Neopetasiger
The 10 sequences from this study all grouped within Neopetasiger sp. 4 and were <1% different in nucleotide identity from Neopetasiger sp. 4 (KM191817), with an average intraspecific divergence of 0.2% and an interspecific divergence of 21.1%–28.2% (Figure 4b and Appendix: Table A6). All Neopetasiger sp. samples from this study were derived from H. trivolvis snails, further indicating their specialization for planorbid snails, as indicated by other studies (Table 3).
3.5.3. Echinoparyphium/Hypoderaeum
All methods in ABGD agreed on separation of the alignment into 17 groups (p max (all) = 0.0129; Figure 5a). This separation was further supported by considering the range of intraspecific divergence values reported previously for several of these same lineages (Detwiler et al., 2016). Furthermore, most groups supported a clear separation of lineages by first‐intermediate host use, confirmed from both Indiana and Alberta. For most lineages, the average within‐group nucleotide divergence was <5%. Despite ABGD results, some lineages with >5% divergence, upon further inspection, revealed evidence for further splitting, including Echinoparyphium sp. Lineage 3 and Hypoderaeum sp. Lineage 1. For example, though ABGD showed Echinoparyphium sp. Lineage 3 to be one group made of four sequences, their p distance values were very divergent. The two sequences from GenBank previously identified as Lineage 3 were 2.7% divergent from each other, but 9.7%–11% divergent from the two sequence from our study that were 3.7% divergent from each other. To us, this was a clear split and was also highly supported by posterior probabilities and bootstrap values in phylogenetic analyses as well. We therefore derived a new lineage, Echinoparyphium sp. Lineage 4.
Figure 5.
Molecular phylogeny of the Echinostomatidae: Echinoparyphium/Hypoderaeum genera based on nad1 and cox1. Bayesian inference phylogenies are given. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 from BI and ML analyses are reported near the nodes, respectively. Accession numbers are given after species names. Clades representing a single species have been condensed for space. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. Emboldened taxa with three asterisks represent novel species from molecular analysis. (a) nad1. (b) cox1
Within the Hypoderaeum sp. Lineage 1 clade, there was an obvious split occurring with three sequences forming their own clade (MGC577, MGC650, and MGC824). This split was not supported by ABGD or by host use, as all utilized S. elodes snails. The nucleotide divergence, however, ranged between 0.3% and 5.4%. The small clade that was found diverging from the rest was 0.3%–0.7% different from each other and 5.0%–5.4% different from the others. The split was obvious and well supported within the phylogenies. We have therefore split this lineage into two groups, now including Hypoderaeum sp. Lineage 2 (Figure 5a).
Several additional new lineages have been added to the genus Echinoparyphium because of our sequencing efforts. We have labeled these as Echinoparyphium sp. A–E, and for the two that are close to the previously identified Echinoparyphium sp. Lineage 1, we have labeled as Echinoparyphium sp. Lineage 1 A–B (Figure 5a).
One group we could not clearly delineate further, despite divergence higher than the cutoff. Echinoparyphium sp. Lineage 2 displayed above 5% intraspecific divergence, with an intraspecific range of 0.0%–5.7% and an average of 1.2%. The one isolate responsible for this greater divergence value is MGC369 that ranges from 1.7% to 5.7% from all other isolates within this lineage. All other isolates in this lineage have an intraspecific divergence range from 0.0% to 4.3% without MGC369. While this difference would seem a clear divergence, the phylogeny does not support the placement of MGC369 outside of this lineage. From host use, we find that MGC369 utilized L. stagnalis, whereas the majority of Lineage 2 isolates used S. elodes. While this would also seem to support differentiation, one other member MGC16B also utilized L. stagnalis, with very close sequence homology to other Lineage 2 members (0.3%–4.3%). Because neither the phylogenies nor host use supports further differentiation for this group, MGC369 remains in this lineage.
The cox1 phylogenies for the Echinostomatidae (Figure 5b), for the most part, were well supported and matched patterns seen within the nad1 phylogenies for this family. Because a few samples had both cox1 and nad1 sequences available, the lineage identities were informed by nad1 because there were not many GenBank cox1 sequences that matched. Overall, there was only one lineage within the cox1 phylogeny that had no overlapping sequences, and these have been labeled broadly as Echinostomatidae gen. sp.
There were two unexpected patterns found within the cox1 phylogeny as compared to the nad1. The lineage we identified as Echinoparyphium sp. Lineage 2 by nad1 had a split, with very large divergence from isolate MGC16B to the other members of the lineage, upwards of 22.7%. Because there were no clear trends to help us understand this difference between the two genes, we have chosen to continue to include it within this same lineage, with the noted caveat.
The other unexpected pattern was within the lineage Echinoparyphium sp. A. Like the previous example, the lineage has split based on the cox1 gene. The range of pairwise distance within this group, including members of both split lineages, was 0.0%–21.4%, with an average intraspecific divergence of 10.5%. Without further evidence, one might conclude that this could be due to oversaturation in cox1, as previously noted for the echinostomes. We did see that one defining feature also separating these clades was intermediate host use. The clade that includes the isolate MGC1143 utilized S. elodes snails, whereas members of the clade with isolate MGC658 all used P. gyrina snails. By nad1, MGC1143 diverged from the other members of this clade by 1.0%–4.7%. MGC658 diverged by 0.3%–3.3%. Both could be considered within an acceptable range, leaving the decision of lump or split nearly impossible based on sequences alone. Host use, especially for the first‐intermediate snail host, is strong evidence that these are more likely to be two different species. In considering that these snails are members of different families and that the only other examples of different snail species being used within other genera of this family utilize species within the same snail family, namely, S. elodes or L. stagnalis, both members of the Lymnaeidae, our best judgment is to split this into two species, based on host use (Appendix: Tables A7 and A8).
3.5.4. Echinostoma
There was strong nodal support by both BI and ML trees for the topology of the Echinostoma species (Figure 6). All ABGD distance methods supported the separation of the alignment into 15 groups (p max (JC & K2) = 0.0359; p max (simple dist.) = 0.02154). Intraspecific divergence values, based on the delineation cutoff, did not always support the same groups. For instance, Echinostoma miyagawai, Echinostoma robustum, and Echinostoma revolutum all exhibited ranges >5%, despite the average being lower, except for E. robustum whose average was 5.4%. Placement of one sequence within the tree did not match expectations but had high statistical support; E. robustum (GQ463053) grouped within a clade of E. miyagawai. The inclusion of the robustum sequence did explain the greater intraspecific divergence within this clade, but there was not support for its placement with the other robustum sequences that also exhibit high intraspecific divergence. Further inspection of this particular robustum sequence has shown previous assessments that have identified this same trend, indeed showing it to be E. miyagawai (Georgieva et al., 2012).
Figure 6.
Molecular phylogeny of the Echinostomatidae based on nad1. Bayesian inference phylogenies are given. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 from BI and ML analyses are reported near the nodes, respectively. Accession numbers are given after species names. Clades representing a single species have been condensed for space. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study
Sequences labeled/identified as Echinostoma trivolvis from GenBank resulted in two paraphyletic groups within the tree, the separation of which was confirmed by ABGD and within‐group divergence values of <5%. These observations confirmed previous lineage separation by Detwiler et al. (2016).
The Echinostoma sequences from the present study all fit within two clades, either E. revolutum or E. trivolvis Lineage A. The revolutum group exhibited higher than expected intraspecific divergence that ranged from 0.0% to 6.0%. Though not supported by ABGD, there did appear to be two separate groups emerging, one that has been found among S. elodes snails (Lineage B) and the other among Lymnaea spp. and ducks (Lineage A). By splitting these lineages, we saw more reasonable intraspecific divergence values within Lineage B (0.0%–1.6%), yet Lineage A continued to exhibit divergence higher than the cutoff (0.0%–5.7%; Appendix: Table A9). Because Lineage B isolates all utilized the same snail host, we were more confident in the grouping of this lineage, but believe that further sampling will likely show greater differentiation within Lineage A.
3.6. Family Diplostomidae
For both Diplostomidae‐I and Diplostomidae‐II groups, BI and ML phylogenies agreed on minor topologies, with greater support for external nodes and less support and agreement between the two methods for internal nodes (Figure 7). For Diplostomidae‐I, all distance methods in ABGD agreed on 41 total groups (p max = 0.059), further supported by the 5% cutoff. A result worth noting from this phylogeny is that a sequence we previously identified as T. scheuringi (KT831356) has now split from this group into a separate, new lineage we are now calling Tylodelphys sp. A. Several sequences from this study did not group specifically with any available GenBank sequences and have formed distinct lineages among the Diplostomum species. These have been identified as Diplostomum spp. A–C (Figure 7 and Appendix: Table A10). Other lineage splits seen within Diplostomum baeri and Tylodelphys sp. 2 have previously been described (Soldánová et al., 2014) and are further supported with our phylogeny.
Figure 7.
Molecular phylogenies of the Diplostomidae‐I Group based on cox1. Clades representing a single species have been condensed for space. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Bootstrap values >50 and posterior probabilities >0.50 are reported near the nodes. Numbers in brackets after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. Emboldened taxa with three asterisks represent novel species from molecular analyses. (a) Maximum‐likelihood tree. (b) Bayesian inference tree
Twenty‐three groups were identified for Diplostomidae‐II, supported by all distance methods of ABGD (p max = 0.059) and the 5% cutoff. Two lineages made up of sequences from this study did not group within a specific clade of previously identified sequences and have thus been identified generally as Diplostomidae gen. sp. O and sp. X. One such sequence was previously identified as being most like Ornithodiplostomum sp. 4 (KT831363); however, in this phylogeny, it grouped far from the other Ornithodiplostomum sequences. Of note is that a sequence from GenBank previously identified as Posthodiplostomum sp. 3 (FJ477217) grouped with high statistical support with sequences of Posthodiplostomum centrarchi (KX931421–KX931423), supporting a very recent report of this same identification (Stoyanov et al., 2018; Figure 8 and Appendix: Table A11).
Figure 8.
Molecular phylogenies of the Diplostomidae‐II Group based on cox1. Clades representing a single species have been condensed for space. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Bootstrap values >50 and posterior probabilities >0.50 are reported near the nodes. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. Emboldened taxa with three asterisks represent novel species from molecular analyses. Black diamonds represent sequences identified uniquely in GenBank that have high similarity and likelihood of being the same as a different species. (a) Maximum‐likelihood tree. (b) Bayesian inference tree
3.7. Family Strigeidae
Few species with sequences across the cox1 barcoding region were available from GenBank for comparison within the Strigeidae‐I group. At the start of our analyses, only two species had matched with some of our sequences, Cotylurus cornutus and Cotylurus gallinulae. More recently, more Cotylurus species have been added to GenBank (Locke et al., 2018), and these additions helped define three previously unidentifiable lineages from phylogenies. Both ML and BI trees agreed with strong statistical support for the division of all aligned sequences into 16 groups, which was further supported by ABGD (p max (all) = 0.0077–0.0129). Sequences from the present study were all more closely related to Cotylurus as opposed to Ichthyocotylurus, based on p distances. Five could be identified to previously named species (C. cornutus, C. gallinulae, Cotylurus flabelliformis, Cotylurus marcogliesei, and Cotylurus strigeoides), and six other lineages did not match to any GenBank sequences and have been identified as Cotylurus sp. A–F. Clade division is further supported by intermediate host use. While intraspecific divergence was within the cutoff for all species, there was lower than expected interspecific divergence between C. cornutus and C. flabelliformis (4.2%; Figure 9a and Appendix: Table A12).
Figure 9.
Molecular phylogenies of the Strigeidae based on cox1. Bayesian inference phylogenies are given. Clades representing a single species have been condensed for space. Branches are colored by support values from phylogenetic analyses, with blue having the highest support. Posterior probabilities >0.50 and bootstrap values >50 are reported near the nodes, respectively. Accession numbers are given after species names. Numbers in parentheses after taxon names correspond to the number of sequences within the clade. The first number is number of GenBank sequences and the second number, if given, represents number of sequences from this study. Emboldened taxa with three asterisks represent novel species from molecular analyses. (a) Strigeidae‐I. (b) Strigeidae‐II
The Strigeidae‐II group utilized the previously published phylogenies of Blasco‐Costa et al. (1977) and Gordy et al. (2013b) as a starting point, with new sequence additions. Unfortunately, there were still no additional species in GenBank to add that would help inform this phylogeny further. However, the addition of new sequences from the present study has revealed even greater diversity than found previously and has supported the previously derived lineages. While both ML and BI trees agreed on topology and provided medium to strong node support, ABGD methods did not agree with the number of groups informed by previous phylogenies or across methods (JC: 26 groups [p max = 0.0077], 21 groups [p max = 0.0129–0.0215], 14 groups [p max = 0.0359]; K2: 26 groups [p max = 0.0129], 21 groups [p max = 0.0215–0.0359], 13 groups [p max = 0.059]; and Simple: 29 groups [p max = 0.007], 28 groups [p max = 0.0129], 18 groups [p max = 0.0215], 13 groups [p max = 0.0359]). Examining divergence based on p distances better supported the phylogenetic results, with 23 groups (including out‐group sequences from Apharyngostrigea spp.) having been within the 5% intraspecific cutoff and having >5% interspecific divergence, all except for Australapatemon burti LIN1, which had an intraspecific divergence range of 0.0%–6.4% and an average of 1.1%. There were only a few sequences that reached the highest part of that range, one new sequence, MGC1629 that came from S. elodes, and five previously published sequences: four from Gordy et al. (2013b) (KY587401, HM385485, KY587400, and HM385486), all cercariae derived from Planorbis sp. snails in California, and JX977727, an adult from Mexico. Though they differed from some other LIN1 sequences >5%, they were more similar to other LIN1 sequences with divergence <5%, which made it difficult to clearly delineate whether there was one monophyletic clade or more. Currently, there is not enough evidence to clearly support more than one clade within Lineage 1.
Therefore, with the best supported information, there appeared to be 23 groups within the Strigeidae‐II, which revealed three new species of Apatemon: species A, which included our previously published Apatemon sp. (KT831859), and species B and C. Though these three species all utilized S. elodes, they were molecularly divergent.
Within the Australapatemon clade, a new lineage appeared from isolate MGC2030 that utilized P. gyrina identified herein as Lineage 10. Lineage 9, with the addition of more sequences, as predicted in Gordy et al. (2013b), has revealed the greater likelihood and separation of this lineage into two, which we have called Lineage 9A and Lineage 9B, both of which were hosted by S. elodes snails (Figure 9b and Appendix: Table A13).
3.8. Species richness and rarefaction
Based on our estimates of species, as described above and evidenced from molecular phylogenies, we have recovered 79 trematode species from five snail host species across six lakes in central Alberta. Richness recoveries were greatest at Isle Lake (38 trematode species/four snail species), followed by Wabamun Lake (27/5), Gull Lake (24/3), Lac La Nonne Site #1 (18/3), Lac La Nonne Site #2 (16/3), Buffalo Lake—Pelican Point (16/3), Buffalo Lake—Rochon Sands (13/2), Buffalo Lake—The Narrows (13/4), and finally, Pigeon Lake Provincial Park (3/1) (Tables 1, 2, 3, 4).
Table 2.
Trematode species counts by collection site
| Buffalo Lake—Pelican Point | Buffalo Lake—Rochon Sands | Buffalo Lake—The Narrows | Gull Lake—Aspen Beach | Isle Lake | Lac La Nonne | Lac La Nonne site #2 | Pigeon Lake—Provincial Park | Wabamun Lake—Provincial Park Beach | Grand total | |
|---|---|---|---|---|---|---|---|---|---|---|
| Apatemon sp. A | – | – | – | – | 16 | – | – | – | – | 16 |
| Apatemon sp. B | – | – | – | – | 1 | – | – | – | – | 1 |
| Apatemon sp. C | – | – | – | – | 4 | – | – | – | – | 4 |
| Australapatemon burti LIN1 | – | – | 2 | 24 | 165 | 2 | 5 | – | 6 | 204 |
| Australapatemon mclaughlini | – | 2 | – | – | – | – | – | – | – | 2 |
| Australapatemon sp. LIN10 | – | – | – | 1 | – | – | – | – | – | 1 |
| Australapatemon sp. LIN3 | – | – | – | 1 | – | – | – | – | – | 1 |
| Australapatemon sp. LIN4 | – | – | – | 1 | – | – | – | – | – | 2 |
| Australapatemon sp. LIN5 | – | 1 | – | – | – | – | – | – | – | 1 |
| Australapatemon sp. LIN6 | – | – | 1 | – | 4 | – | 1 | 1 | – | 7 |
| Australapatemon sp. LIN8 | 1 | 4 | – | 1 | 3 | – | – | – | – | 9 |
| Australapatemon sp. LIN9A | – | 2 | – | 7 | 6 | 2 | – | – | – | 17 |
| Australapatemon sp. LIN9B | 3 | 1 | – | – | – | – | – | – | – | 4 |
| Avian schistosomatid sp. A | – | 3 | 2 | – | 2 | – | – | – | – | 7 |
| Avian schistosomatid sp. B | – | – | – | – | – | – | 1 | – | – | 1 |
| Avian schistosomatid sp. C | – | – | – | – | – | – | – | – | 1 | 1 |
| Bolbophorus sp. | – | – | 6 | – | 2 | – | – | – | 2 | 10 |
| Cotylurus cornutus | – | – | – | 2 | 32 | – | 1 | – | – | 35 |
| Cotylurus flabelliformis | – | – | – | – | 1 | – | – | – | – | 1 |
| Cotylurus marcogliesei | 1 | – | – | 3 | 2 | 1 | – | – | – | 7 |
| Cotylurus sp. A | – | – | – | – | 34 | 1 | 1 | – | 3 | 39 |
| Cotylurus sp. B | – | – | – | – | 1 | – | – | – | – | 1 |
| Cotylurus sp. C | – | – | 3 | – | – | – | – | – | – | 3 |
| Cotylurus sp. D | – | 1 | – | – | – | – | – | – | – | 1 |
| Cotylurus sp. E | 2 | 1 | – | 2 | 5 | 2 | – | – | – | 12 |
| Cotylurus sp. F | – | – | 4 | – | – | – | – | – | 2 | 6 |
| Cotylurus strigeoides | – | 1 | 1 | – | 11 | 1 | 6 | – | 2 | 22 |
| Diplostomidae gen. sp. O | 6 | 19 | – | 6 | 2 | – | – | – | 1 | 34 |
| Diplostomidae gen. sp. X | – | – | – | – | 1 | – | – | – | – | 1 |
| Diplostomum baeri LIN2 | – | – | – | – | 3 | – | – | – | 2 | 5 |
| Diplostomum indistinctum | – | – | – | 1 | – | – | – | – | – | 1 |
| Diplostomum sp. 1 | – | – | – | – | 1 | – | – | – | 5 | 6 |
| Diplostomum sp. 3 | – | – | – | – | – | – | – | – | 3 | 3 |
| Diplostomum sp. 4 | 9 | – | – | 7 | 24 | – | 1 | – | 30 | 71 |
| Diplostomum sp. A | 1 | – | – | – | – | – | – | – | – | 1 |
| Diplostomum sp. B | – | – | – | – | 1 | – | – | – | – | 1 |
| Diplostomum sp. C | – | – | – | 1 | 10 | – | – | – | 1 | 12 |
| Drepanocephalus spathans | – | – | 3 | – | 1 | – | – | – | – | 4 |
| Echinoparyphium sp. A | 2 | – | – | 4 | 22 | 2 | 7 | 2 | 7 | 46 |
| Echinoparyphium sp. A2 | – | – | – | 4 | – | 2 | 1 | – | – | 7 |
| Echinoparyphium sp. B | – | – | – | – | – | 9 | – | – | – | 9 |
| Echinoparyphium sp. C | – | – | – | 8 | – | 16 | 1 | – | – | 25 |
| Echinoparyphium sp. D | 1 | – | – | – | – | – | – | – | – | 1 |
| Echinoparyphium sp. E | – | – | – | 6 | – | – | – | – | – | 6 |
| Echinoparyphium sp. Lineage 1A | – | – | – | – | 10 | 18 | 46 | – | 23 | 97 |
| Echinoparyphium sp. Lineage 1B | – | – | – | – | 1 | – | – | – | – | 1 |
| Echinoparyphium sp. Lineage 2 | 12 | 1 | – | 29 | 13 | 27 | 4 | – | 3 | 89 |
| Echinoparyphium sp. Lineage 4 | – | – | 1 | – | – | – | – | – | 1 | 2 |
| Echinostoma revolutum B | 11 | – | – | 11 | 2 | 7 | 1 | – | 1 | 33 |
| Echinostoma trivolvis Lineage A | – | – | – | – | 2 | 2 | – | – | 1 | 5 |
| Echinostomatidae gen. sp. | 4 | – | – | – | – | – | – | – | – | 4 |
| Haematoloechidae gen. sp. A | 4 | – | – | – | – | – | – | – | – | 4 |
| Hypoderaeum sp. Lineage 1 | – | – | – | 5 | – | – | – | – | 1 | 6 |
| Hypoderaeum sp. Lineage 2 | – | – | – | – | 1 | 2 | – | – | – | 3 |
| Neodiplostomum americanum | 1 | – | – | – | – | – | – | – | – | 1 |
| Neopetasiger islandicus | – | – | – | – | – | – | – | – | 1 | 1 |
| Neopetasiger sp. 4 | – | – | 1 | – | 2 | – | – | – | 7 | 10 |
| Notocotylus sp. A | 1 | 1 | – | 1 | 12 | 9 | 6 | – | 9 | 39 |
| Notocotylus sp. B | – | – | – | – | – | – | – | – | 1 | 1 |
| Notocotylus sp. C | –– | – | – | – | – | 1 | – | – | – | 1 |
| Notocotylus sp. D | 4 | 1 | – | 21 | 23 | 4 | 1 | – | – | 54 |
| Ornithodiplostomum sp. 2 | – | – | –– | – | – | – | – | – | 1 | 1 |
| Ornithodiplostomum sp. 8 | – | – | – | – | 3 | – | – | 1 | – | 4 |
| Plagiorchis sp.a | 343 | 78 | 58 | 257 | 173 | 132 | 26 | – | 78 | 1,145 |
| Posthodiplostomum sp. 4 | – | – | – | – | 2 | – | – | – | – | 2 |
| Psilostomidae gen. sp. A | – | –– | – | – | 4 | – | – | – | 2 | 6 |
| Schistosomatium douthitti | – | – | 6 | 3 | – | – | – | – | 1 | 10 |
| Trichobilharzia physellae | – | – | – | – | – | 1 | – | – | – | 1 |
| Trichobilharzia stagnicolae | – | – | – | – | 8 | – | – | – | – | 8 |
| Trichobilharzia szidati | – | – | 1 | 1 | – | – | – | – | – | 2 |
| Tylodelphys sp. A | – | – | – | – | – | – | – | – | 5 | 5 |
| Grand total | 406 | 116 | 89 | 407 | 610 | 241 | 110 | 4 | 200 | 2,183 |
Includes all lineages.
Table 4.
Snail host–trematode parasite relationships from this study
| Helisoma trivolvis | Lymnaea stagnalis | Physa gyrina | Planorbula armigera | Stagnicola elodes | Grand total | |
|---|---|---|---|---|---|---|
| Apatemon sp. A | – | – | – | – | 16 | 16 |
| Apatemon sp. B | – | – | – | – | 1 | 1 |
| Apatemon sp. C | – | – | – | – | 4 | 4 |
| Australapatemon burti LIN1 | 2 | 1 | 2 | – | 199 | 204 |
| Australapatemon mclaughlini | – | – | 2 | – | – | 2 |
| Australapatemon sp. LIN10 | – | – | 1 | – | – | 1 |
| Australapatemon sp. LIN3 | – | – | – | – | 1 | 1 |
| Australapatemon sp. LIN4 | – | – | 2 | – | – | 2 |
| Australapatemon sp. LIN5 | – | – | – | – | 1 | 1 |
| Australapatemon sp. LIN6 | – | – | 7 | – | – | 7 |
| Australapatemon sp. LIN8 | – | – | 9 | – | – | 9 |
| Australapatemon sp. LIN9A | – | 1 | – | – | 16 | 17 |
| Australapatemon sp. LIN9B | – | – | – | – | 4 | 4 |
| Avian schistosomatid sp. A | – | – | 7 | – | – | 7 |
| Avian schistosomatid sp. B | – | – | 1 | – | – | 1 |
| Avian schistosomatid sp. C | 1 | – | – | – | – | 1 |
| Bolbophorus sp. | 10 | – | – | – | – | 10 |
| Cotylurus cornutus | 1 | – | – | – | 32 | 33 |
| Cotylurus flabelliformis | – | – | – | – | 1 | 1 |
| Cotylurus marcogliesei | – | – | – | – | 5 | 5 |
| Cotylurus sp. A | – | – | 1 | – | 38 | 39 |
| Cotylurus sp. B | – | – | 1 | – | – | 1 |
| Cotylurus sp. C | – | 3 | – | – | – | 3 |
| Cotylurus sp. D | – | – | 1 | – | – | 1 |
| Cotylurus sp. E | – | – | – | – | 11 | 11 |
| Cotylurus sp. F | – | 6 | – | – | – | 6 |
| Cotylurus strigeoides | – | – | 21 | – | 1 | 22 |
| Diplostomidae gen. sp. O | – | – | 34 | – | – | 34 |
| Diplostomidae gen. sp. X | – | – | 1 | – | – | 1 |
| Diplostomum baeri LIN2 | – | – | – | – | 5 | 5 |
| Diplostomum indistinctum | – | – | – | – | 1 | 1 |
| Diplostomum sp. 1 | – | – | – | – | 6 | 6 |
| Diplostomum sp. 3 | – | 3 | – | – | – | 3 |
| Diplostomum sp. 4 | – | – | – | – | 71 | 71 |
| Diplostomum sp. A | – | – | – | – | 1 | 1 |
| Diplostomum sp. B | – | – | – | – | 1 | 1 |
| Diplostomum sp. C | 1 | – | – | – | 11 | 12 |
| Drepanocephalus spathans | 4 | – | – | – | – | 4 |
| Echinoparyphium sp. A | – | – | 44 | – | 2 | 46 |
| Echinoparyphium sp. A2 | – | – | 1 | – | 6 | 7 |
| Echinoparyphium sp. B | – | – | – | – | 9 | 9 |
| Echinoparyphium sp. C | – | – | – | – | 25 | 25 |
| Echinoparyphium sp. D | – | – | – | – | 1 | 1 |
| Echinoparyphium sp. E | – | 1 | – | – | 5 | 6 |
| Echinoparyphium sp. Lineage 1A | 1 | – | 94 | – | 2 | 97 |
| Echinoparyphium sp. Lineage 1B | – | – | 1 | – | – | 1 |
| Echinoparyphium sp. Lineage 2 | 1 | 3 | – | – | 80 | 84 |
| Echinoparyphium sp. Lineage 4 | 2 | – | – | – | – | 2 |
| Echinostoma revolutum B | – | – | – | – | 33 | 33 |
| Echinostoma trivolvis Lineage A | 5 | – | – | – | – | 5 |
| Echinostomatidae gen. sp. | – | – | – | – | 4 | 4 |
| Haematoloechidae gen. sp. A | – | – | – | – | 4 | 4 |
| Hypoderaeum sp. Lineage 1 | – | – | – | – | 5 | 5 |
| Hypoderaeum sp. Lineage 2 | – | – | – | – | 3 | 3 |
| Neodiplostomum americanum | – | – | – | – | 1 | 1 |
| Neopetasiger islandicus | – | – | – | 1 | – | 1 |
| Neopetasiger sp. 4 | 10 | – | – | – | – | 10 |
| Notocotylus sp. A | – | – | 36 | – | 3 | 39 |
| Notocotylus sp. B | – | – | 1 | – | – | 1 |
| Notocotylus sp. C | 1 | – | – | – | – | 1 |
| Notocotylus sp. D | – | – | 5 | – | 45 | 50 |
| Ornithodiplostomum sp. 2 | – | – | 1 | – | – | 1 |
| Ornithodiplostomum sp. 8 | – | – | 4 | – | – | 4 |
| Plagiorchis sp.a | 7 | 89 | 12 | – | 1,027 | 1,135 |
| Posthodiplostomum sp. 4 | – | – | 2 | – | – | 2 |
| Psilostomidae gen. sp. A | 6 | – | – | – | – | 6 |
| Schistosomatium douthitti | – | 8 | – | – | 2 | 10 |
| Trichobilharzia physellae | – | – | 1 | – | – | 1 |
| Trichobilharzia stagnicolae | – | – | – | – | 8 | 8 |
| Trichobilharzia szidati | – | 2 | – | – | – | 2 |
| Tylodelphys sp. A | 5 | – | – | – | – | 5 |
| Grand total | 57 | 117 | 292 | 1 | 1,691 | 2,158 |
Includes all lineages.
Of the 79 total trematode species reported here, 59 are newly identified species in this report that have resulted in 15 updated identifications for previously published sequences (Table 3). Thirty‐nine of the 59 new identifications represent novel lineages/singletons (represented by “a” in Table 3), with another two lineages that represent a recent split (Australapatemon sp. LIN9A/9B). The remaining 20 species were previously identified, and for 15 of them, we have added further sequenced specimens, confirming their previous identifications and adding to our understanding of species presence and abundances in Alberta lakes (Table 3 and Appendix: Table A14).
Examining the relationship of trematode species richness and sample size (by sites/area and individuals) through rarefaction and nonlinear models revealed a stark contrast between whether confidence for delimitation was at a family‐level (morphological analysis) or a species‐level (molecular analysis; Figure 10a–c). Considering the accumulation of trematode families, the curves plateaued (individual‐based) or approached one (site‐based), suggesting we likely captured the available trematode families within our samples and sample region. However, when looking at the curves based on trematode species accumulation, there was no plateau, suggesting that there was potentially greater trematode species diversity than we captured from our sampling. Snails, on the other hand, plateaued in rarefaction analyses (Figure 10d,e). This was not at all surprising, considering that over 3 years of collections, we had yet to find more than seven species.
Figure 10.
Species accumulation. Several methods confirm that if delineation confidence for species differences is based on morphological identification, a plateau is reached for the maximum number of species within the study area. Whereas if confidence is based on molecular phylogenetic methods, we have yet to attain the true diversity of trematode species within the study area. (a) Collector method for accumulating sites as in the dataset, (b) Rarefaction for number of individuals, (c) Random method for accumulating sites given as a boxplot, with nonlinear Arrhenius model results displayed as lines behind the boxplot, (d) Rarefaction for number of individuals by snail species, (e) Random method for accumulating sites given as a boxplot for snail species
The greatest richness recoveries by snail host species were found among S. elodes (40 trematode species), followed by P. gyrina (26), H. trivolvis (15), L. stagnalis (10), and P. armigera (1), following the same trend as identified previously (Gordy et al., 2013a), but with more total species (Table 5). Specificity for snail host species was high (55 specialist trematode species) among all but 15 trematodes, of which were found to infect two or more snail species (generalists). Some trematodes were found infecting snails from completely different families, these were A. burti LIN1 (S. elodes, L. stagnalis, H. trivolvis, P. gyrina), Echinoparyphium sp. LIN1A (S. elodes, H. trivolvis, P. gyrina), and Notocotylus sp. A/D (S. elodes, P. gyrina).
Table 5.
Summary of representation for digenean mitochondrial genes in GenBank
| Order | Family | No. of cox1 seq. | No. of spp. | Named spp. | No. of nad1 seq. | No. of spp. | Named spp. |
|---|---|---|---|---|---|---|---|
| Strigeidida | Schistosomatidae | 1,434 | 104 | 46 | 523 | 16 | 15 |
| Diplostomidae | 1,079 | 110 | 20 | 3 | 3 | ||
| Clinostimidae | 390 | 29 | 11 | 1 | 1 | ||
| Strigeidae | 188 | 46 | 18 | 20 | 7 | ||
| Bucephalidae | 66 | 5 | |||||
| Leuchochloridae | 31 | 6 | 11 | 4 | |||
| Bolbophoridae | 15 | 5 | |||||
| Aporocotylidae | 10 | 10 | |||||
| Cyathocotylidae | 9 | 1 | |||||
| Spirorchiidae | 5 | 5 | |||||
| Fellodistomidae | 5 | 3 | 12 | 11 | |||
| Leuchochloridiomorphidae | 1 | 1 | |||||
| Panopstidae | 1 | 1 | |||||
| Plagiorchiida | Fasciolidae | 463 | 31 | 4 | 533 | 45 | 7 |
| Opecoelidae | 416 | 24 | 7 | 203 | 2 | 2 | |
| Troglotrematidae | 333 | 24 | 7 | 35 | 6 | ||
| Apocreadiidae | 261 | 5 | 4 | ||||
| Echinostomatidae | 228 | 23 | 10 | 344 | 51 | 28 | |
| Microphallidae | 158 | 6 | |||||
| Allocreadiiidae | 143 | 13 | |||||
| Dicrocoeliidae | 115 | 15 | 33 | 6 | |||
| Himasthlidae | 79 | 9 | |||||
| Monorchiidae | 69 | 17 | |||||
| Plagiorchiidae | 64 | 19 | 16 | ||||
| Gorgoderidae | 61 | 17 | |||||
| Haematoloechidae | 52 | 23 | 15 | ||||
| Paramphistomidae | 49 | 14 | 34 | 5 | |||
| Notocotylidae | 42 | 8 | 2 | 2 | 2 | ||
| Gymnophallidae | 41 | 3 | |||||
| Brachycladiidae | 39 | 3 | |||||
| Lepocreadiidae | 39 | 1 | 46 | 40 | |||
| Philophthalmidae | 38 | 5 | 20 | 3 | |||
| Collyriclidae | 37 | 1 | 8 | 1 | |||
| Gastrothylacidae | 23 | 6 | 2 | 2 | |||
| Renicolidae | 21 | 8 | 6 | 4 | |||
| Pleurogenidae | 15 | 2 | |||||
| Prosthogonimidae | 14 | 4 | 16 | 4 | |||
| Gorgocephalidae | 8 | 1 | |||||
| Psilostomidae | 5 | 4 | 3 | ||||
| Callodistomidae | 4 | 4 | |||||
| Paramphistomatidae | 3 | 3 | |||||
| Telorchiidae | 2 | 2 | |||||
| Alloglossidiidae | 2 | 1 | 177 | 23 | 17 | ||
| Cephalogonimidae | 2 | 1 | |||||
| Lissorchiidae | 2 | 2 | |||||
| Echinochasmidae | 1 | 1 | 1 | 1 | |||
| Olveriidae | 1 | 1 | |||||
| Opisthorchiida | Heterophyidae | 680 | 29 | 20 | 3 | 2 | |
| Opisthorchiidae | 469 | 13 | 12 | 28 | 8 | ||
| Cryptogonimidae | 66 | 3 | 1 | 1 | |||
| Acanthocolpidae | 1 | 1 | 1 | 1 | |||
| Azygiida | Didymozoidae | 82 | 2 | ||||
| Derogenidae | 14 | 5 | |||||
| Accacoeliidae | 5 | 2 | |||||
| Azygiidae | 3 | 3 | |||||
| Hirudinellidae | 2 | 2 | |||||
| Hemiuridae | 1 | 1 | |||||
| Isoparorchiidae | 1 | 1 |
4. DISCUSSION
Fine‐scale molecular analyses of trematodes in central Alberta have revealed many new and important insights about their diversity. What is perhaps most surprising is that species accumulation curves would suggest we have yet to capture all the possible trematode species within our sample area. Comparing the species‐level to family‐level accumulation clearly demonstrates how important the molecular phylogenetic perspective is. Herein, we have used the family‐level as a proxy for the type of results achieved by morphological analysis only, in considering trematode larval stages. While morphological identification of trematode larvae can be less costly in terms of materials, it does not afford a very high level of confidence because of the issues surrounding cryptic species and underdeveloped, definable features. Family‐level accumulation based on individuals and sites is achieved at a much higher rate than species, as expected, and reaches a plateau earlier. If, for instance, this representation is true of the number of species attained by a typical survey, it is likely that trematode surveys are missing much of the actual diversity present. This is important to note because of the potential impact on how we might interpret community assembly and structure in natural environments, especially in consideration of cryptic species.
Overall, the trematode species richness found by this longitudinal survey exceeded expectations, and the number of snail species needed in a community to maintain a diverse set of trematodes was surprisingly small. In our original morphological assessments, we expected 29 trematode species. With the use of molecular assessments, based on BLAST identities and fewer sequenced samples, generated from the first 2 years of the study, we had expanded our view to 39 identified species (Gordy et al., 2013a). Now, with more available sequence information, and the use of more stringent methods, we have, in total, recovered double the species from previous assessments at a total of 79 trematode species, 55 of which are new records to Alberta from this study alone. This raises the recorded trematode species in Alberta to 114, representing 16 families (Appendix: Table A14).
For an ecoregion that has previously been considered species‐poor (Hoberg, Galbreath, Cook, Kutz, & Polley, 1993b), sub‐Arctic lake ecosystems have presented a surprising amount of trematode diversity from recent surveys. From one lake in Norway, on the 69th parallel, 24 different trematode species were recovered, representing seven different, common families from lakes in the Northern hemisphere (e.g., Strigeidae, Diplostomidae, Schistosomatidae, Echinostomatidae, Notocotylidae, Plagiorchiidae; Soldánová et al., 2014). Though further South, between the 54th and 52nd parallel, our study is still considered within the sub‐Arctic region and has uncovered a range of 3–38 trematode species representing 3–8 families, each, among six lakes (the lower end, from Pigeon Lake and Lac La Nonne, was only sampled in 1 year as opposed to 3 years for the other lakes). In between, sampling of fish from the Saint Lawrence River in Quebec (between the 49th and 44th parallel) has revealed 47 species of just diplostomoids (Locke, Mclaughlin et al., 2010). From these surveys, it is apparent that our perspective of what constitutes incredible or unexpected diversity is changing and will continue to change as we take a closer look with molecular data. In all three of these studies, the unveiling of cryptic diversity has been a large component. From a recent meta‐analysis of 110 studies, it has been noted that there is a trend, particularly among trematodes, that sequencing effort positively correlates with more cryptic species as opposed to any other group of helminths. This has been attributed to differences in trematode biology, and our ability as taxonomists to identify them by their morphological characters, or lack thereof (Pérez‐Ponce de León & Poulin, 2010b).
From a basic search of the GenBank database, we can see that trematodes are not a neglected group, as there are 877,472 molecular records specific to digeneans (as of August 2018). However, this is not to say that specific groups of digenean are not neglected nor that representation is not highly skewed to particular gene regions or to those species most important to human or veterinary health. Of the digenean sequences in GenBank, 15,185 were of mitochondrial origin. Considering the two most used mitochondrial genes for barcoding digeneans, we limited our search to cox1 and nad1 (ND1), finding that a few families were represented by more than 400 sequences, some having more nad1 than cox1 or vice versa, and this was not consistent with the estimated number of genera or species within the family. For instance, the family Fasciolidae was found to have 463 cox1 sequences that represented 31 unnamed species (uniquely identified in GenBank) and four named species. This family was also represented by 533 nad1 sequences representing 45 molecular species and seven named species. Considering that previous assessments have only identified eight potential species in this family (Cribb et al., 2016), this is incredible coverage. Other families, though, have nearly 900 species, like the Opecoelidae (Bray, Cribb, Littlewood, & Waeschenbach, 2017), and have a similar breadth of species and sequences as the Fasciolidae, showing them to be greatly underrepresented (Table 5).
In this study, the relevant trematode families with the best cox1/nad1 coverage from GenBank were the Echinostomatidae, Strigeidae, and Diplostomidae. Despite many genera being represented within these families, there remain many gaps in species identifications. This was apparent through a large variety of unidentified species lineages. Unfortunately, our study has only widened this gap, by identifying even more novel, unidentified species lineages and singletons because we lack molecular evidence from adult worms. However, these efforts are not in vain, as they provide a foundation for further sampling that may create the missing life cycle links between larvae and adults in the future. For instance, the species C. marcogliesei was just described for the first time this past year (Locke et al., 2018), based on adult worms derived from a Hooded Merganser in Montreal, QC. The alignment of our sequences to that of Locke et al. have now added a new snail first‐intermediate host record, S. elodes, in addition to a new geographical record of being in Alberta. Considering that Cotylurus spp. have been described as having snails as a second‐intermediate host, it is possible for them to use the same species, although typically not the exact same snail individual (Graczyk & Shiff, 2014). Meaning that further sampling of S. elodes may uncover metacercariae of C. marcogliesei. Overall, there is further opportunity for this species’ second‐intermediate host to be discovered to complete our understanding of the life cycle and host use within.
The trematode families found in Alberta that need greater sampling and effort from both adult worms and molecular barcoding are the Notocotylidae, Psilostomidae, Haematoloechidae, and most importantly, the Plagiorchiidae. The Plagiorchiidae are the most abundant family found in central Alberta lakes, and there is statistical evidence, through phylogenetics presented herein, for the presence of at least nine species. This family is said to be composed of at least 100 species (Blankespoor, 2013). Furthermore, Plagiorchis spp. have been indicated as vectors for Potomac Horse Fever (Vaughan, Tkach, & Greiman, 2016), which has been diagnosed among several horses near Edmonton, Alberta (personal communication with horse owners, and positive sequence identifications of Neorickettsia risticii, unpublished).
In the Notocotylidae, we identified four species, but all were provisionally named species A–D because, as with many of our samples, there was no clear evidence to connect them to any previously identified species, and the evidence found was quite disparate. From the literature, only two named species have been identified in Canada, including Notocotylus attenuatus (Quebec and Manitoba) and N. urbanensis (previously N. filamentis) (British Columbia and Ontario), and three others have been identified in the Nearctic region, N. linearis, N. pacifier, and N. stagnicolae. Broadly, these species infect Anatids and aquatic mammals like muskrats (multiple references found in Gibson, Bray, & Harris, 2016). Prior evidence related to their snail hosts is limited to records from the United States: N. attenuatus has been identified from Physa acuta in the Eastern United States (Graczyk & Shiff, 2005), and N. urbanensis was identified from Stagnicola emarginata in Michigan (Keas & Blankespoor, 2017). No records to our knowledge have thus far indicated P. gyrina, S. elodes, or H. trivolvis as intermediate hosts for Notocotylus species. The only records of any Notocotylus spp. in Alberta previously have been unnamed species found in the shorebirds Recurvirostra americana and Catoptrophorus semipalmatus (Gibson et al., 2016). Considering that we cannot link these unknown species in shorebirds to our samples, the four species we have identified can be considered new geographical and host records for Notocotylids. A final note about this family is the need for further sampling among Stagnicola and Physa snail species in Alberta as an effort to further define Notocotylus sp. A and D. These two species have lower interspecific divergence between them than between the other species in the family and exhibit mixed host use, with preference for one host over the other and that happen to be opposite of each other. We speculate that this may be evidence of a current speciation event in which increased host preferences are leading to specialization and resulting in their division, at least on a molecular level.
Both Haematoloechidae and Psilostomidae species were difficult to identify for several reasons. The first reason was that either there were not very many cox1 sequences available for comparison or the sequences available for that gene were from an upstream region and did not overlap. The other reason was that there have been no previous records of species from either family in Alberta or many records in general from snail hosts, and none from snails within Canada. While lymnaeid snails have previously been indicated as intermediate hosts for Haematoloechus spp. (Gibson et al., 2016), to our knowledge, none have been specifically identified from S. elodes. Several other snail families (Physidae and Planorbidae) are also hosts for different species of Haematoloechus, indicating they do not specialize by snail family, but could specialize for snail species, which may be regionally determined (Gibson et al., 2016). For both families, records within Canada have all come from the Eastern provinces (Quebec, Ontario, New Brunswick, and Nova Scotia) and from definitive hosts (Psilostomidae: Anatid birds and aquatic mammals; Haematoloechidae: frogs; Gibson et al., 2016). It is impossible at this point to know whether the presence of species from these families is from recent introductions or not, but they are rare in the fact that we only collected a few from each family over the course of 3 years. Considering their host species are quite prevalent across Alberta, it is possible that they have been here and remained undetected, but they could also have expanded their distributions westward into Alberta as well.
The gap between morphological and molecular species identities is growing larger, and the effort to find a solution is not growing at the same rate. Without the link between the two, we are missing important information about life cycle dynamics due to host associations and infection processes that could help inform wildlife managers and possibly influence control efforts for human and veterinary diseases caused by trematodes. One possible solution to this, aside from more molecular data from adult worm samples, is the development of methods to derive quality sequence information from historical, adult trematode specimens. As these vouchers have been our historical standard for species identifications, they are our ultimate source for generating molecular libraries by which to further our understanding of trematode diversity, speciation, and evolution with the added benefit of linking life cycles.
Furthermore, we urge the contribution of sequences that represent a broader diversity of digenean trematodes. One current issue is that novel lineages in molecular phylogenies could either represent cryptic species or they could represent described species for which we have no/limited molecular resources. Therefore, placing emphasis on capturing a broader diversity of trematodes might help bridge knowledge gaps.
CONFLICT OF INTEREST
None declared.
AUTHOR CONTRIBUTIONS
MAG designed and performed the research, completed all analyses, and wrote the paper. PCH was involved with conception and design of the research, reviewing the results, and contributed to writing the paper.
ACKNOWLEDGMENTS
We would like to acknowledge Elisabeth Richardson and Joel Dacks for fruitful discussion surrounding phylogenetic analyses, and Valerie K. Philips for assistance with fieldwork. We thank Sean A. Locke, Janet Koprivnikar, and Jillian T. Detwiler for an early review of the manuscript, as well as three anonymous reviewers for their constructive comments. This work was funded by Alberta Innovates Energy and Environment Solutions grant 2078 and NSERC 418540 (PCH), with partial salary support for MAG by an NSERC CREATE Host‐Parasite Interactions student scholarship.
APPENDIX A.
A.1.
Table 6.
Average cox1 divergence within and between groups in the Notocotylidae. The number of base differences per site from between sequences are shown. Standard error estimate(s) are shown above the diagonal. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 98 nucleotide sequences. Codon positions included were 1st + 2nd + 3rd + Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 322 positions in the final dataset. Standard error estimates are shown above the diagonal. Average within group divergence is given on the diagonal. Group intraspecific divergence ranges are given as percentages next to species names. Numbers in red are outside the delineation cut‐off
| E. hortense | N. sp. A | N. sp. B | N. sp. C | N. sp. D | O. sikae | |
|---|---|---|---|---|---|---|
| Echinostoma hortense (out) | ‐ | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 |
| Notocotylus sp. A (0.0–4.3%) | 0.274 | 0.013 | 0.012 | 0.014 | 0.008 | 0.020 |
| Notocotylus sp. B | 0.270 | 0.059 | ‐ | 0.016 | 0.014 | 0.020 |
| Notocotylus sp. C | 0.261 | 0.083 | 0.102 | ‐ | 0.014 | 0.021 |
| Notocotylus sp. D (0.0–4.3%) | 0.273 | 0.038 | 0.084 | 0.088 | 0.013 | 0.020 |
| Ogmocotyle sikae | 0.258 | 0.188 | 0.196 | 0.208 | 0.198 | ‐ |
Table 7.
Pairwise distance between individual cox1 sequences in the Psilostomidae. The number of base differences per site from between sequences are shown. Standard error estimate(s) are shown above the diagonal. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 11 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 496 positions in the final dataset
| MGC342 | MGC2085 | MGC2089 | MGC406 | KT831366 | MGC1319 | E. japonicus | P. varium | S. globulus | S. pseudoglobulus | S. pseudoglobulus | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Psilostomatidae gen. sp. A*** MGC342 | 0.004 | 0.004 | 0.004 | 0.004 | 0.004 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Psilostomatidae gen. sp. A*** MGC2085 | 0.010 | 0.000 | 0.002 | 0.002 | 0.002 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Psilostomatidae gen. sp. A*** MGC2089 | 0.010 | 0.000 | 0.002 | 0.002 | 0.002 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Psilostomatidae gen. sp. A*** MGC406 | 0.008 | 0.002 | 0.002 | 0.000 | 0.000 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Psilostomatidae gen. sp. A *** KT831366 | 0.008 | 0.002 | 0.002 | 0.000 | 0.000 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Psilostomatidae gen. sp. A*** MGC1319 | 0.008 | 0.002 | 0.002 | 0.000 | 0.000 | 0.018 | 0.015 | 0.019 | 0.019 | 0.019 | |
| Echinochasmus japonicus (out) | 0.234 | 0.234 | 0.234 | 0.236 | 0.236 | 0.236 | 0.018 | 0.018 | 0.018 | 0.018 | |
| Pseudopsilostoma varium | 0.143 | 0.145 | 0.145 | 0.147 | 0.147 | 0.147 | 0.230 | 0.019 | 0.018 | 0.018 | |
| Sphaeridiotrema globulus | 0.242 | 0.244 | 0.244 | 0.246 | 0.246 | 0.246 | 0.228 | 0.258 | 0.018 | 0.018 | |
| Sphaeridiotrema pseudoglobulus | 0.244 | 0.246 | 0.246 | 0.244 | 0.244 | 0.244 | 0.232 | 0.254 | 0.192 | 0.000 | |
| Sphaeridiotrema pseudoglobulus | 0.244 | 0.246 | 0.246 | 0.244 | 0.244 | 0.244 | 0.232 | 0.254 | 0.192 | 0.000 |
Table 8.
Pairwise distance between individual cox1 sequences in the Haematoloechidae. The number of base differences per site from between sequences are shown. Standard error estimate(s) are shown above the diagonal. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 7 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 454 positions in the final dataset
| KT831372 | MGC1782 | MGC1787 | MGC1792 | H. sp. 9781 | H.sp. 9782 | Plagiorchis sp. | |
|---|---|---|---|---|---|---|---|
| Haematoloechidae gen. sp. A***KT831372 | 0.000 | 0.000 | 0.000 | 0.016 | 0.018 | 0.020 | |
| Haematoloechidae gen. sp. A***MGC1782 | 0.000 | 0.000 | 0.000 | 0.016 | 0.018 | 0.020 | |
| Haematoloechidae gen. sp. A ***MGC1787 | 0.000 | 0.000 | 0.000 | 0.016 | 0.018 | 0.020 | |
| Haematoloechidae gen. sp. A***MGC1792 | 0.000 | 0.000 | 0.000 | 0.016 | 0.018 | 0.020 | |
| Haematoloechus sp. BOLD:ACK9781 | 0.134 | 0.134 | 0.134 | 0.134 | 0.019 | 0.020 | |
| Haematoloechus sp. BOLD:ACK9782 | 0.207 | 0.207 | 0.207 | 0.207 | 0.216 | 0.019 | |
| Plagiorchis sp. (out) FJ477214 | 0.240 | 0.240 | 0.240 | 0.240 | 0.258 | 0.218 |
Table 9.
Average cox1 divergence within and between groups of Plagiorchis sp. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. The average within group divergence is given on the diagonal. The range of pairwise distances within each group are given as percentages in the first column after group names. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 55 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 435 positions in the final dataset
| P. sp. LIN1 | P. sp. LIN2 | P. sp. LIN3 | P. sp. LIN4 | P. sp. LIN5 | P. sp. LIN6 | P. sp. LIN7 | P. sp. LIN8 | P. sp. LIN9 | |
|---|---|---|---|---|---|---|---|---|---|
| Plagiorchis sp. LIN1 (0.0–2.3%) | 0.010 | 0.017 | 0.017 | 0.015 | 0.016 | 0.017 | 0.017 | 0.017 | 0.016 |
| Plagiorchis sp. LIN2 | 0.165 | ‐ | 0.017 | 0.017 | 0.016 | 0.017 | 0.016 | 0.018 | 0.017 |
| Plagiorchis sp. LIN3 (0.2–0.7%) | 0.148 | 0.178 | 0.005 | 0.016 | 0.017 | 0.017 | 0.017 | 0.017 | 0.018 |
| Plagiorchis sp. LIN4 (0.0–0.7%) | 0.123 | 0.145 | 0.140 | 0.003 | 0.015 | 0.016 | 0.016 | 0.016 | 0.016 |
| Plagiorchis sp. LIN5 (0.2–0.5%) | 0.148 | 0.152 | 0.173 | 0.121 | 0.003 | 0.016 | 0.015 | 0.017 | 0.017 |
| Plagiorchis sp. LIN6 | 0.169 | 0.156 | 0.162 | 0.143 | 0.149 | ‐ | 0.016 | 0.016 | 0.016 |
| Plagiorchis sp. LIN7 (0.0–0.7%) | 0.157 | 0.158 | 0.162 | 0.149 | 0.125 | 0.143 | 0.004 | 0.017 | 0.017 |
| Plagiorchis sp. LIN8 (0.2–1.8%) | 0.166 | 0.188 | 0.180 | 0.140 | 0.159 | 0.151 | 0.154 | 0.013 | 0.012 |
| Plagiorchis sp. LIN9 (0.0–1.1%) | 0.151 | 0.167 | 0.171 | 0.142 | 0.150 | 0.155 | 0.155 | 0.089 | 0.005 |
Table 10.
Pairwise distance between individual nad1 sequences in the genus Drepanocephalus . The number of base differences per site from between sequences are shown. Standard error estimate(s) are shown above the diagonal. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 6 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 388 positions in the final dataset
| F. hepatica | MGC2147 | MGC2353 | D. auritus | D. auritus | Drep. sp. | |
|---|---|---|---|---|---|---|
| Fasciola hepatica (out) | 0.021 | 0.021 | 0.021 | 0.022 | 0.021 | |
| MGC2147: MH368951 | 0.227 | 0.000 | 0.000 | 0.010 | 0.018 | |
| MGC2353: MH368952 | 0.227 | 0.000 | 0.000 | 0.010 | 0.018 | |
| Drepanocephalus auritus KP053262 | 0.227 | 0.000 | 0.000 | 0.010 | 0.018 | |
| Drepanocephalus auritus KP053263 | 0.235 | 0.044 | 0.044 | 0.044 | 0.018 | |
| Drepanocephalus sp. KP053264 | 0.245 | 0.144 | 0.144 | 0.144 | 0.155 |
Table 11.
Average nad1 divergence within and between genera of Neopetasiger . The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. On the diagonal are the average within group divergence estimates. The range of pairwise distances within groups is given in parentheses next to the group names. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 20 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 308 positions in the final dataset
| N. islandic. | N. necome. | Neop.sp. 1 | Neop.sp. 2 | Neop.sp. 3 | Neop.sp. 4 | |
|---|---|---|---|---|---|---|
| Neopetasiger islandicus | ‐ | 0.025 | 0.020 | 0.019 | 0.021 | 0.022 |
| Neopetasiger necomense | 0.286 | ‐ | 0.026 | 0.026 | 0.025 | 0.024 |
| Neopetasiger sp. 1 | 0.172 | 0.325 | 0.000 | 0.020 | 0.023 | 0.025 |
| Neopetasiger sp. 2 | 0.143 | 0.318 | 0.149 | 0.000 | 0.022 | 0.024 |
| Neopetasiger sp. 3 (0.3–1.3%) | 0.162 | 0.298 | 0.231 | 0.193 | 0.900 | 0.022 |
| Neopetasiger sp. 4 (0.0–0.7%) | 0.211 | 0.276 | 0.282 | 0.240 | 0.214 | 0.200 |
Table 12.
Average nad1 divergence within and between genera of Echinoparyphium/Hypoderaeum . The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. Intraspecific divergence values are given on the diagonal. The range of p distances is given for each group in parentheses as percentages after species names. Numbers highlighted in red are above the 5% cut‐off, while numbers in green represent average interspecific divergence below 5%. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 261 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 299 positions in the final dataset
| E. aconia. | Ec. ellisi | Ec. poulini | Ec. recurv. | Ec. sp. A | Ec. sp. A2 | Ec. sp. B | Ec. sp. C | Ec. sp. D | Ec. sp. E | Ec. sp. L1 | Ec. sp. L1A | Ec. sp. L1B | Ec. sp. L2 | Ec. sp. L3 | Ec. sp. L4 | H. conoid. | H. sp. LIN1 | H. sp. LIN2 | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Echinoparyphium aconiatum | 0.000 | 0.023 | 0.024 | 0.025 | 0.023 | 0.022 | 0.024 | 0.023 | 0.023 | 0.022 | 0.023 | 0.025 | 0.024 | 0.022 | 0.023 | 0.023 | 0.023 | 0.023 | 0.024 |
| Ec. ellisi | 0.204 | 0.000 | 0.022 | 0.022 | 0.021 | 0.021 | 0.025 | 0.024 | 0.024 | 0.025 | 0.019 | 0.021 | 0.021 | 0.020 | 0.022 | 0.022 | 0.024 | 0.023 | 0.024 |
| Ec. poulini | 0.207 | 0.171 | 0.000 | 0.023 | 0.022 | 0.023 | 0.027 | 0.025 | 0.024 | 0.025 | 0.022 | 0.022 | 0.021 | 0.020 | 0.023 | 0.022 | 0.024 | 0.024 | 0.025 |
| Ec. recurvatum (0.7–1.7%) | 0.239 | 0.196 | 0.202 | 0.011 | 0.024 | 0.023 | 0.026 | 0.025 | 0.025 | 0.025 | 0.022 | 0.023 | 0.022 | 0.021 | 0.023 | 0.022 | 0.024 | 0.023 | 0.024 |
| Echinoparyphium sp. A (0.0–5.0%) | 0.193 | 0.176 | 0.170 | 0.221 | 0.019 | 0.010 | 0.025 | 0.024 | 0.023 | 0.024 | 0.021 | 0.021 | 0.021 | 0.020 | 0.019 | 0.019 | 0.022 | 0.022 | 0.022 |
| Echinoparyphium sp. A2 | 0.181 | 0.167 | 0.181 | 0.204 | 0.044 | ‐ | 0.025 | 0.023 | 0.023 | 0.024 | 0.021 | 0.022 | 0.022 | 0.021 | 0.020 | 0.019 | 0.023 | 0.023 | 0.023 |
| Echinoparyhium sp. B (0.0–1.3%) | 0.215 | 0.241 | 0.268 | 0.271 | 0.233 | 0.228 | 0.004 | 0.020 | 0.023 | 0.022 | 0.025 | 0.025 | 0.025 | 0.026 | 0.026 | 0.025 | 0.025 | 0.025 | 0.024 |
| Echinoparyphium sp. C (3.7%) | 0.194 | 0.221 | 0.227 | 0.242 | 0.220 | 0.204 | 0.161 | 0.037 | 0.021 | 0.022 | 0.024 | 0.026 | 0.024 | 0.024 | 0.024 | 0.023 | 0.024 | 0.024 | 0.024 |
| Echinoparyphium sp. D | 0.217 | 0.221 | 0.227 | 0.231 | 0.214 | 0.204 | 0.218 | 0.187 | ‐ | 0.021 | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 | 0.024 | 0.024 | 0.025 |
| Echinoparyphium sp. E (0.0–1.3%) | 0.179 | 0.247 | 0.232 | 0.258 | 0.224 | 0.210 | 0.193 | 0.171 | 0.164 | 0.008 | 0.023 | 0.024 | 0.025 | 0.023 | 0.024 | 0.023 | 0.024 | 0.025 | 0.025 |
| Echinoparyphium sp. LIN1 (2.0–3.0%) | 0.202 | 0.144 | 0.173 | 0.200 | 0.178 | 0.172 | 0.250 | 0.241 | 0.224 | 0.223 | 0.025 | 0.014 | 0.017 | 0.019 | 0.021 | 0.021 | 0.023 | 0.022 | 0.023 |
| Echinoparyphium sp. LIN1A (0.0–1.0%) | 0.233 | 0.156 | 0.188 | 0.216 | 0.169 | 0.183 | 0.251 | 0.255 | 0.230 | 0.227 | 0.086 | 0.002 | 0.018 | 0.020 | 0.021 | 0.021 | 0.024 | 0.024 | 0.024 |
| Echinoparyphium sp. LIN1B | 0.214 | 0.171 | 0.171 | 0.201 | 0.184 | 0.181 | 0.255 | 0.239 | 0.227 | 0.235 | 0.111 | 0.120 | ‐ | 0.020 | 0.022 | 0.020 | 0.022 | 0.022 | 0.022 |
| Echinoparyphium sp. LIN2 (0.0–5.7%) | 0.184 | 0.145 | 0.143 | 0.174 | 0.164 | 0.171 | 0.262 | 0.222 | 0.210 | 0.216 | 0.154 | 0.157 | 0.161 | 0.012 | 0.022 | 0.020 | 0.022 | 0.022 | 0.023 |
| Echinoparyphium sp. LIN3 (2.7%) | 0.199 | 0.184 | 0.187 | 0.212 | 0.146 | 0.151 | 0.255 | 0.236 | 0.234 | 0.222 | 0.174 | 0.188 | 0.194 | 0.190 | 0.027 | 0.017 | 0.023 | 0.023 | 0.023 |
| Echinoparyphium sp. LIN4 (3.7%) | 0.196 | 0.174 | 0.157 | 0.181 | 0.152 | 0.145 | 0.242 | 0.217 | 0.212 | 0.209 | 0.173 | 0.176 | 0.174 | 0.158 | 0.105 | 0.037 | 0.024 | 0.024 | 0.024 |
| Hypoderaeum conoideum | 0.204 | 0.227 | 0.211 | 0.227 | 0.206 | 0.214 | 0.251 | 0.232 | 0.244 | 0.227 | 0.215 | 0.230 | 0.201 | 0.195 | 0.226 | 0.217 | ‐ | 0.014 | 0.015 |
| Hypoderaeum sp. LIN1 (0.0–1.7%) | 0.196 | 0.218 | 0.219 | 0.226 | 0.199 | 0.205 | 0.252 | 0.239 | 0.239 | 0.236 | 0.204 | 0.214 | 0.189 | 0.191 | 0.223 | 0.221 | 0.069 | 0.008 | 0.011 |
| Hypoderaeum sp. LIN2 (0.3–0.7%) | 0.221 | 0.227 | 0.227 | 0.222 | 0.198 | 0.204 | 0.229 | 0.237 | 0.241 | 0.247 | 0.217 | 0.223 | 0.196 | 0.208 | 0.229 | 0.224 | 0.077 | 0.048 | 0.004 |
Table 13.
Average cox1 divergence within and between genera of Echinostomatidae. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. Intraspecific divergence is given on the diagonal. Numbers in red represent groups that exceed the cut‐off. The range of p‐distances is given for each group in parentheses as percentages after species names. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 111 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 383 positions in the final dataset
| D. auritus | D. mexican. | D. spathans | E. trivolvis | E. gen. sp. | E. revol.B | Ec.gen.sp.2 | Ec.sp.A2 | Ec.sp.A | Ec.sp.C | Ec.sp.E | Ec.sp.L1A | Ec.sp.L2 | Ec.sp.L3 | H. conoid. | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Drepanocephalus auritus (0.0–2.9%) | 0.006 | 0.016 | 0.009 | 0.020 | 0.021 | 0.021 | 0.022 | 0.021 | 0.019 | 0.021 | 0.021 | 0.020 | 0.018 | 0.021 | 0.021 |
| Drepanocephalus mexicanus (2.3%) | 0.129 | 0.023 | 0.016 | 0.020 | 0.020 | 0.020 | 0.022 | 0.020 | 0.019 | 0.020 | 0.020 | 0.020 | 0.018 | 0.019 | 0.020 |
| Drepanocephalus spathans (0.0%) | 0.036 | 0.132 | 0.000 | 0.020 | 0.020 | 0.021 | 0.022 | 0.021 | 0.020 | 0.020 | 0.020 | 0.021 | 0.019 | 0.021 | 0.021 |
| Echinostoma trivolvis | 0.261 | 0.270 | 0.256 | ‐ | 0.014 | 0.017 | 0.022 | 0.019 | 0.019 | 0.019 | 0.018 | 0.018 | 0.017 | 0.018 | 0.018 |
| Echinostomatidae gen. sp. | 0.293 | 0.273 | 0.279 | 0.097 | ‐ | 0.016 | 0.022 | 0.019 | 0.018 | 0.018 | 0.017 | 0.018 | 0.017 | 0.018 | 0.018 |
| Echinostoma revolutum Lineage B (0.0–1.8%) | 0.265 | 0.273 | 0.261 | 0.150 | 0.140 | 0.010 | 0.022 | 0.019 | 0.018 | 0.019 | 0.018 | 0.018 | 0.015 | 0.018 | 0.018 |
| Echinostomatidae gen. sp. 2 (0.0–0.5%) | 0.309 | 0.294 | 0.305 | 0.275 | 0.272 | 0.265 | 0.003 | 0.021 | 0.021 | 0.020 | 0.021 | 0.022 | 0.020 | 0.021 | 0.022 |
| Echinoparyphium sp. A2 (0.0–1.6%) | 0.253 | 0.247 | 0.242 | 0.199 | 0.206 | 0.203 | 0.261 | 0.006 | 0.019 | 0.017 | 0.018 | 0.018 | 0.017 | 0.019 | 0.019 |
| Ecchinoparyphium sp. A (0.0–3.7%) | 0.240 | 0.245 | 0.249 | 0.188 | 0.191 | 0.187 | 0.260 | 0.206 | 0.018 | 0.019 | 0.019 | 0.016 | 0.014 | 0.016 | 0.019 |
| Echinoparyphium sp. C (0.0–1.3%) | 0.251 | 0.241 | 0.250 | 0.209 | 0.184 | 0.194 | 0.258 | 0.167 | 0.207 | 0.007 | 0.018 | 0.019 | 0.017 | 0.019 | 0.018 |
| Echinoparyphium sp. E (0.8%) | 0.253 | 0.255 | 0.256 | 0.176 | 0.158 | 0.187 | 0.243 | 0.185 | 0.190 | 0.155 | 0.008 | 0.018 | 0.017 | 0.018 | 0.019 |
| Echinoparyphium sp. LIN1 A (0.0–1.6%) | 0.247 | 0.247 | 0.251 | 0.162 | 0.170 | 0.179 | 0.269 | 0.186 | 0.142 | 0.204 | 0.182 | 0.003 | 0.014 | 0.015 | 0.019 |
| Echinoparyphium sp. LIN2 (0.3–22.7%) | 0.267 | 0.260 | 0.272 | 0.197 | 0.197 | 0.184 | 0.282 | 0.227 | 0.164 | 0.206 | 0.211 | 0.141 | 0.114 | 0.014 | 0.017 |
| Echinoparyphium sp. LIN3 | 0.243 | 0.240 | 0.240 | 0.170 | 0.175 | 0.181 | 0.257 | 0.187 | 0.132 | 0.195 | 0.172 | 0.127 | 0.145 | ‐ | 0.019 |
| Hypoderaeum conoideum | 0.261 | 0.272 | 0.261 | 0.188 | 0.196 | 0.206 | 0.269 | 0.201 | 0.205 | 0.187 | 0.181 | 0.191 | 0.209 | 0.185 | ‐ |
Table 14.
Average nad1 divergence within and between groups of Echinostoma spp. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. The average within group divergence is given on the diagonal. The range of pairwise distances within each group are given as percentages in the first column after group names. Numbers in red lie outside the delineation cut‐off. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 72 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 386 positions in the final dataset
| E. bolsch. | E. caproni | E. desert. | E. friedi/IG | E. miyag. | E. nasinc. | E. novaze. | E. paraen. | E. paraul. | E. rev. A | E. rev. B | E. robust. | Echino. sp. | E. triv. A | E. triv. B | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Echinostoma bolschwense (0.3%) | 0.003 | 0.019 | 0.018 | 0.019 | 0.018 | 0.018 | 0.018 | 0.019 | 0.018 | 0.017 | 0.017 | 0.017 | 0.021 | 0.017 | 0.017 |
| Echinostoma caproni (2.8%) | 0.181 | 0.028 | 0.017 | 0.019 | 0.016 | 0.018 | 0.016 | 0.017 | 0.016 | 0.017 | 0.017 | 0.016 | 0.021 | 0.016 | 0.017 |
| Echinostoma deserticum | 0.152 | 0.162 | ‐ | 0.020 | 0.017 | 0.018 | 0.017 | 0.019 | 0.017 | 0.017 | 0.017 | 0.017 | 0.021 | 0.017 | 0.018 |
| Echinostoma friedi/IG (0.3–0.5%) | 0.191 | 0.201 | 0.217 | 0.003 | 0.019 | 0.020 | 0.020 | 0.020 | 0.020 | 0.020 | 0.020 | 0.019 | 0.021 | 0.020 | 0.020 |
| Echinostoma miyagawai (0.8–5.2%) | 0.164 | 0.136 | 0.149 | 0.194 | 0.031 | 0.017 | 0.014 | 0.017 | 0.015 | 0.014 | 0.014 | 0.012 | 0.021 | 0.016 | 0.016 |
| Echinostoma nasincovae (0.3%) | 0.161 | 0.154 | 0.166 | 0.201 | 0.148 | 0.003 | 0.017 | 0.016 | 0.018 | 0.016 | 0.016 | 0.016 | 0.021 | 0.015 | 0.014 |
| Echinostoma novazealandense (0.0–0.3%) | 0.143 | 0.120 | 0.139 | 0.205 | 0.092 | 0.120 | 0.002 | 0.017 | 0.015 | 0.014 | 0.015 | 0.014 | 0.022 | 0.016 | 0.016 |
| Echinostoma paraensei (0.3%) | 0.174 | 0.141 | 0.180 | 0.195 | 0.151 | 0.114 | 0.135 | 0.003 | 0.017 | 0.017 | 0.018 | 0.016 | 0.021 | 0.017 | 0.016 |
| Echinostoma paraulum (0.5%) | 0.159 | 0.141 | 0.145 | 0.196 | 0.106 | 0.150 | 0.111 | 0.141 | 0.005 | 0.015 | 0.016 | 0.014 | 0.020 | 0.016 | 0.017 |
| Echinostoma revolutum Lineage A (0.0–5.7%) | 0.137 | 0.139 | 0.133 | 0.197 | 0.107 | 0.123 | 0.086 | 0.148 | 0.125 | 0.010 | 0.010 | 0.014 | 0.021 | 0.015 | 0.016 |
| Echinostoma revolutum Lineage B (0.0–1.6%) | 0.147 | 0.144 | 0.144 | 0.196 | 0.102 | 0.126 | 0.098 | 0.154 | 0.125 | 0.052 | 0.007 | 0.014 | 0.022 | 0.015 | 0.015 |
| Echinostoma robustum (5.4%) | 0.154 | 0.145 | 0.155 | 0.200 | 0.079 | 0.131 | 0.098 | 0.139 | 0.096 | 0.106 | 0.109 | 0.054 | 0.021 | 0.015 | 0.015 |
| Echinostoma sp. | 0.237 | 0.245 | 0.246 | 0.262 | 0.251 | 0.255 | 0.261 | 0.250 | 0.233 | 0.250 | 0.256 | 0.255 | ‐ | 0.021 | 0.021 |
| Echinostoma trivolvis Lineage A (0.0–1.3%) | 0.148 | 0.140 | 0.152 | 0.190 | 0.134 | 0.097 | 0.123 | 0.120 | 0.136 | 0.115 | 0.120 | 0.126 | 0.237 | 0.006 | 0.012 |
| Echinostoma trivolvis Lineage B (0.3–2.8%) | 0.140 | 0.164 | 0.180 | 0.207 | 0.143 | 0.098 | 0.125 | 0.129 | 0.148 | 0.127 | 0.127 | 0.125 | 0.250 | 0.080 | 0.018 |
Table 15.
Average cox1 divergence within and between genera of Diplostomidae-I. The number of base differences per site from averaging over all sequence pairs between groups are shown below the diagonal. Standard error estimate(s) are shown above the diagonal. On the diagonal are the average within group divergence values. Numbers within parentheses after species names represent the range of percent divergence within groups. Species with three asterisks represent novel species by molecular phylogeny. The analysis involved 196 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 334 positions in the final dataset
| A. ostrow. | Alar. sp. 1 | Alar. sp. 2 | D. ardeae | D. b. LIN1 | D. b LIN2 | D. huron. | D. indist. | D. mergi | D. parvi. | D. pseudo. | Dipl. sp. 1 | Dipl. sp. 2 | Dipl. sp. 4 | Dipl. sp. 6 | Dipl. sp. 7 | Dipl. sp. 8 | Dipl. sp. 9 | Dipl. sp. A | Dipl. sp. B | Dipl. sp. C | Dipl. cladeQ | D. sp.LIN6 | D. spath. | T. aztecae | T.clavata | T. excav. | T. immer | T. jenyns. | T. masho. | T. scheur. | T. sp. 2LIN1 | T. sp. 2LIN2 | T. sp. 3 | T. sp. 4 | T. sp. 5 | T. sp. 6 | T. sp. A | T. sp. IBC | T. sp. IND | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Austrodiplostomum ostrowskiae (0.3–0.9%) | 0.006 | 0.017 | 0.016 | 0.018 | 0.020 | 0.020 | 0.019 | 0.020 | 0.020 | 0.019 | 0.018 | 0.020 | 0.020 | 0.020 | 0.019 | 0.019 | 0.020 | 0.021 | 0.020 | 0.020 | 0.020 | 0.020 | 0.020 | 0.019 | 0.020 | 0.020 | 0.018 | 0.018 | 0.017 | 0.020 | 0.018 | 0.020 | 0.018 | 0.019 | 0.019 | 0.019 | 0.017 | 0.018 | 0.016 | 0.017 |
| Alaria sp. 1 | 0.100 | ‐ | 0.017 | 0.018 | 0.020 | 0.019 | 0.019 | 0.020 | 0.021 | 0.020 | 0.019 | 0.020 | 0.020 | 0.020 | 0.020 | 0.021 | 0.020 | 0.019 | 0.019 | 0.021 | 0.019 | 0.021 | 0.020 | 0.021 | 0.018 | 0.020 | 0.019 | 0.017 | 0.019 | 0.020 | 0.019 | 0.020 | 0.018 | 0.018 | 0.019 | 0.020 | 0.019 | 0.017 | 0.018 | 0.018 |
| Alaria sp. 2 (0.0%) | 0.098 | 0.099 | 0.000 | 0.021 | 0.021 | 0.021 | 0.020 | 0.021 | 0.020 | 0.020 | 0.020 | 0.020 | 0.019 | 0.021 | 0.021 | 0.021 | 0.021 | 0.021 | 0.021 | 0.020 | 0.022 | 0.021 | 0.021 | 0.021 | 0.020 | 0.020 | 0.019 | 0.019 | 0.018 | 0.019 | 0.019 | 0.020 | 0.019 | 0.019 | 0.019 | 0.020 | 0.018 | 0.019 | 0.017 | 0.019 |
| Diplostomum ardeae | 0.137 | 0.144 | 0.162 | ‐ | 0.019 | 0.019 | 0.018 | 0.017 | 0.016 | 0.017 | 0.017 | 0.018 | 0.018 | 0.017 | 0.017 | 0.017 | 0.016 | 0.018 | 0.017 | 0.018 | 0.017 | 0.018 | 0.019 | 0.016 | 0.018 | 0.018 | 0.017 | 0.017 | 0.019 | 0.018 | 0.018 | 0.020 | 0.017 | 0.016 | 0.018 | 0.018 | 0.018 | 0.016 | 0.015 | 0.017 |
| Diplostomum baeri LIN1 (0.9%) | 0.146 | 0.169 | 0.184 | 0.136 | 0.009 | 0.018 | 0.018 | 0.019 | 0.019 | 0.018 | 0.017 | 0.019 | 0.017 | 0.018 | 0.016 | 0.015 | 0.019 | 0.019 | 0.019 | 0.018 | 0.019 | 0.018 | 0.017 | 0.018 | 0.020 | 0.020 | 0.020 | 0.020 | 0.020 | 0.020 | 0.019 | 0.022 | 0.020 | 0.019 | 0.020 | 0.020 | 0.020 | 0.020 | 0.019 | 0.020 |
| Diplostomum baeri LIN2 (0.0–0.9%) | 0.152 | 0.150 | 0.170 | 0.137 | 0.125 | 0.004 | 0.017 | 0.019 | 0.018 | 0.018 | 0.017 | 0.018 | 0.019 | 0.016 | 0.017 | 0.017 | 0.018 | 0.019 | 0.018 | 0.019 | 0.016 | 0.018 | 0.019 | 0.018 | 0.019 | 0.020 | 0.018 | 0.020 | 0.020 | 0.019 | 0.020 | 0.020 | 0.018 | 0.020 | 0.019 | 0.019 | 0.019 | 0.019 | 0.020 | 0.020 |
| Diplostomum huronense (0.3–0.6%) | 0.147 | 0.145 | 0.157 | 0.128 | 0.117 | 0.102 | 0.004 | 0.016 | 0.016 | 0.014 | 0.017 | 0.017 | 0.017 | 0.017 | 0.015 | 0.017 | 0.019 | 0.018 | 0.018 | 0.017 | 0.016 | 0.016 | 0.016 | 0.015 | 0.019 | 0.019 | 0.017 | 0.017 | 0.019 | 0.019 | 0.019 | 0.018 | 0.018 | 0.017 | 0.017 | 0.017 | 0.019 | 0.018 | 0.018 | 0.018 |
| Diplostomum indistinctum (0.3–0.9%) | 0.171 | 0.167 | 0.176 | 0.132 | 0.147 | 0.148 | 0.096 | 0.005 | 0.017 | 0.016 | 0.016 | 0.016 | 0.017 | 0.017 | 0.018 | 0.019 | 0.019 | 0.018 | 0.018 | 0.019 | 0.017 | 0.018 | 0.019 | 0.014 | 0.019 | 0.020 | 0.019 | 0.018 | 0.019 | 0.020 | 0.019 | 0.021 | 0.019 | 0.019 | 0.019 | 0.019 | 0.020 | 0.018 | 0.019 | 0.019 |
| Diplostomum mergi (0.0–2.4%) | 0.158 | 0.170 | 0.157 | 0.113 | 0.149 | 0.134 | 0.101 | 0.121 | 0.016 | 0.013 | 0.016 | 0.016 | 0.017 | 0.016 | 0.018 | 0.018 | 0.018 | 0.018 | 0.016 | 0.018 | 0.017 | 0.016 | 0.017 | 0.016 | 0.019 | 0.018 | 0.018 | 0.018 | 0.017 | 0.019 | 0.017 | 0.020 | 0.017 | 0.018 | 0.018 | 0.018 | 0.017 | 0.018 | 0.017 | 0.018 |
| Diplostomum parviventosum (0.6%) | 0.151 | 0.165 | 0.164 | 0.107 | 0.134 | 0.133 | 0.086 | 0.114 | 0.069 | 0.006 | 0.017 | 0.017 | 0.015 | 0.016 | 0.017 | 0.018 | 0.018 | 0.018 | 0.016 | 0.017 | 0.017 | 0.016 | 0.016 | 0.015 | 0.019 | 0.019 | 0.018 | 0.017 | 0.017 | 0.019 | 0.018 | 0.018 | 0.018 | 0.017 | 0.017 | 0.017 | 0.018 | 0.017 | 0.017 | 0.018 |
| Diplostomum pseudospathaceum (0.0–3.3%) | 0.138 | 0.157 | 0.163 | 0.128 | 0.126 | 0.119 | 0.109 | 0.114 | 0.117 | 0.124 | 0.018 | 0.015 | 0.017 | 0.015 | 0.018 | 0.017 | 0.017 | 0.017 | 0.017 | 0.018 | 0.016 | 0.018 | 0.018 | 0.013 | 0.018 | 0.020 | 0.017 | 0.019 | 0.019 | 0.019 | 0.018 | 0.020 | 0.018 | 0.018 | 0.018 | 0.019 | 0.016 | 0.017 | 0.018 | 0.020 |
| Diplostomum sp. 1 (0.0–1.5%) | 0.160 | 0.150 | 0.151 | 0.139 | 0.146 | 0.138 | 0.102 | 0.096 | 0.112 | 0.116 | 0.095 | 0.007 | 0.017 | 0.018 | 0.018 | 0.018 | 0.018 | 0.019 | 0.017 | 0.018 | 0.017 | 0.018 | 0.018 | 0.015 | 0.018 | 0.019 | 0.017 | 0.019 | 0.020 | 0.019 | 0.019 | 0.021 | 0.018 | 0.019 | 0.019 | 0.018 | 0.019 | 0.019 | 0.018 | 0.020 |
| Diplostomum sp. 2 | 0.146 | 0.156 | 0.150 | 0.123 | 0.114 | 0.133 | 0.109 | 0.125 | 0.114 | 0.092 | 0.119 | 0.110 | ‐ | 0.018 | 0.016 | 0.016 | 0.018 | 0.018 | 0.017 | 0.016 | 0.018 | 0.017 | 0.017 | 0.017 | 0.019 | 0.019 | 0.019 | 0.019 | 0.019 | 0.019 | 0.019 | 0.021 | 0.019 | 0.018 | 0.020 | 0.019 | 0.018 | 0.018 | 0.018 | 0.020 |
| Diplostomum sp. 4 (0.0–1.5%) | 0.156 | 0.153 | 0.166 | 0.120 | 0.126 | 0.098 | 0.097 | 0.119 | 0.106 | 0.107 | 0.093 | 0.120 | 0.122 | 0.004 | 0.018 | 0.018 | 0.017 | 0.016 | 0.017 | 0.018 | 0.017 | 0.018 | 0.017 | 0.015 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.017 | 0.017 | 0.018 | 0.018 | 0.019 | 0.017 | 0.019 | 0.020 |
| Diplostomum sp. 6 | 0.137 | 0.156 | 0.177 | 0.111 | 0.102 | 0.104 | 0.094 | 0.131 | 0.138 | 0.119 | 0.131 | 0.133 | 0.102 | 0.131 | ‐ | 0.015 | 0.017 | 0.020 | 0.019 | 0.018 | 0.018 | 0.019 | 0.017 | 0.017 | 0.020 | 0.020 | 0.019 | 0.019 | 0.019 | 0.020 | 0.020 | 0.020 | 0.018 | 0.018 | 0.019 | 0.020 | 0.019 | 0.019 | 0.018 | 0.019 |
| Diplostomum sp. 7 | 0.135 | 0.162 | 0.174 | 0.117 | 0.084 | 0.110 | 0.115 | 0.158 | 0.137 | 0.140 | 0.120 | 0.139 | 0.099 | 0.129 | 0.078 | ‐ | 0.018 | 0.019 | 0.019 | 0.017 | 0.018 | 0.019 | 0.017 | 0.017 | 0.019 | 0.019 | 0.019 | 0.020 | 0.021 | 0.020 | 0.020 | 0.020 | 0.019 | 0.020 | 0.020 | 0.020 | 0.019 | 0.019 | 0.019 | 0.020 |
| Diplostomum sp. 8 | 0.161 | 0.156 | 0.171 | 0.099 | 0.141 | 0.119 | 0.124 | 0.137 | 0.123 | 0.125 | 0.112 | 0.121 | 0.108 | 0.114 | 0.111 | 0.126 | ‐ | 0.017 | 0.018 | 0.018 | 0.016 | 0.018 | 0.015 | 0.017 | 0.018 | 0.019 | 0.018 | 0.019 | 0.019 | 0.019 | 0.018 | 0.020 | 0.018 | 0.018 | 0.018 | 0.020 | 0.018 | 0.019 | 0.018 | 0.020 |
| Diplostomum sp. 9 | 0.170 | 0.147 | 0.174 | 0.135 | 0.138 | 0.149 | 0.128 | 0.138 | 0.130 | 0.124 | 0.124 | 0.136 | 0.123 | 0.109 | 0.150 | 0.138 | 0.114 | ‐ | 0.019 | 0.019 | 0.016 | 0.018 | 0.016 | 0.017 | 0.019 | 0.021 | 0.020 | 0.019 | 0.019 | 0.020 | 0.019 | 0.021 | 0.020 | 0.019 | 0.020 | 0.020 | 0.019 | 0.019 | 0.019 | 0.020 |
| Diplostomum sp. A*** | 0.149 | 0.144 | 0.165 | 0.123 | 0.141 | 0.137 | 0.126 | 0.132 | 0.118 | 0.114 | 0.127 | 0.109 | 0.117 | 0.123 | 0.141 | 0.138 | 0.132 | 0.132 | ‐ | 0.018 | 0.017 | 0.017 | 0.019 | 0.017 | 0.020 | 0.019 | 0.019 | 0.019 | 0.020 | 0.019 | 0.019 | 0.021 | 0.018 | 0.019 | 0.020 | 0.019 | 0.020 | 0.017 | 0.019 | 0.019 |
| Diplostomum sp. B*** | 0.153 | 0.168 | 0.159 | 0.138 | 0.120 | 0.135 | 0.112 | 0.143 | 0.125 | 0.111 | 0.122 | 0.125 | 0.090 | 0.135 | 0.129 | 0.111 | 0.120 | 0.135 | 0.132 | ‐ | 0.017 | 0.018 | 0.017 | 0.017 | 0.020 | 0.018 | 0.019 | 0.020 | 0.020 | 0.020 | 0.020 | 0.021 | 0.020 | 0.020 | 0.020 | 0.019 | 0.019 | 0.019 | 0.019 | 0.020 |
| Diplostomum sp. C ***(0.0–2.1%) | 0.157 | 0.149 | 0.179 | 0.114 | 0.141 | 0.103 | 0.111 | 0.125 | 0.120 | 0.113 | 0.107 | 0.112 | 0.117 | 0.111 | 0.125 | 0.132 | 0.092 | 0.101 | 0.108 | 0.112 | 0.005 | 0.017 | 0.017 | 0.017 | 0.019 | 0.019 | 0.018 | 0.019 | 0.019 | 0.019 | 0.020 | 0.021 | 0.019 | 0.019 | 0.020 | 0.019 | 0.019 | 0.019 | 0.019 | 0.019 |
| Diplostomum sp. clade Q | 0.163 | 0.180 | 0.189 | 0.123 | 0.130 | 0.128 | 0.097 | 0.129 | 0.111 | 0.107 | 0.123 | 0.130 | 0.114 | 0.117 | 0.138 | 0.144 | 0.129 | 0.129 | 0.123 | 0.132 | 0.112 | ‐ | 0.017 | 0.017 | 0.019 | 0.019 | 0.018 | 0.018 | 0.019 | 0.020 | 0.019 | 0.019 | 0.019 | 0.018 | 0.018 | 0.018 | 0.019 | 0.017 | 0.018 | 0.019 |
| Diplostomum sp. LIN6 (0.3–1.8%) | 0.171 | 0.171 | 0.180 | 0.150 | 0.124 | 0.136 | 0.106 | 0.139 | 0.123 | 0.109 | 0.129 | 0.121 | 0.111 | 0.120 | 0.120 | 0.128 | 0.085 | 0.108 | 0.148 | 0.116 | 0.107 | 0.118 | 0.012 | 0.018 | 0.018 | 0.020 | 0.019 | 0.018 | 0.019 | 0.020 | 0.019 | 0.020 | 0.020 | 0.018 | 0.017 | 0.019 | 0.018 | 0.019 | 0.019 | 0.020 |
| Diplostomum spathaceum (0.3–2.1%) | 0.155 | 0.171 | 0.189 | 0.115 | 0.128 | 0.139 | 0.089 | 0.092 | 0.112 | 0.105 | 0.088 | 0.095 | 0.115 | 0.091 | 0.122 | 0.127 | 0.117 | 0.111 | 0.110 | 0.128 | 0.120 | 0.120 | 0.128 | 0.011 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.019 | 0.018 | 0.021 | 0.019 | 0.018 | 0.018 | 0.017 | 0.019 | 0.018 | 0.017 | 0.018 |
| Tylodelphys aztecae (0.6–1.5%) | 0.159 | 0.138 | 0.163 | 0.129 | 0.157 | 0.137 | 0.145 | 0.159 | 0.160 | 0.156 | 0.131 | 0.141 | 0.147 | 0.132 | 0.152 | 0.140 | 0.132 | 0.152 | 0.166 | 0.164 | 0.142 | 0.158 | 0.141 | 0.143 | 0.010 | 0.020 | 0.018 | 0.017 | 0.020 | 0.019 | 0.017 | 0.020 | 0.019 | 0.017 | 0.018 | 0.018 | 0.018 | 0.018 | 0.017 | 0.020 |
| Tylodelphys clavata (0.6–1.2%) | 0.156 | 0.146 | 0.157 | 0.131 | 0.161 | 0.167 | 0.145 | 0.173 | 0.145 | 0.163 | 0.158 | 0.155 | 0.149 | 0.160 | 0.160 | 0.144 | 0.145 | 0.178 | 0.149 | 0.146 | 0.165 | 0.156 | 0.170 | 0.157 | 0.154 | 0.008 | 0.017 | 0.020 | 0.019 | 0.018 | 0.018 | 0.018 | 0.018 | 0.019 | 0.019 | 0.016 | 0.019 | 0.019 | 0.018 | 0.018 |
| Tylodelphys excavata | 0.123 | 0.138 | 0.135 | 0.120 | 0.156 | 0.132 | 0.109 | 0.155 | 0.136 | 0.137 | 0.123 | 0.114 | 0.144 | 0.135 | 0.141 | 0.144 | 0.129 | 0.159 | 0.150 | 0.141 | 0.135 | 0.138 | 0.139 | 0.132 | 0.132 | 0.111 | ‐ | 0.018 | 0.018 | 0.017 | 0.018 | 0.018 | 0.017 | 0.016 | 0.018 | 0.015 | 0.017 | 0.018 | 0.015 | 0.019 |
| Tylodelphys immer (0.3–0.6%) | 0.132 | 0.121 | 0.151 | 0.127 | 0.168 | 0.143 | 0.113 | 0.133 | 0.138 | 0.133 | 0.153 | 0.143 | 0.144 | 0.126 | 0.151 | 0.157 | 0.147 | 0.151 | 0.139 | 0.162 | 0.143 | 0.128 | 0.132 | 0.136 | 0.125 | 0.147 | 0.126 | 0.004 | 0.016 | 0.017 | 0.016 | 0.018 | 0.018 | 0.014 | 0.017 | 0.016 | 0.018 | 0.015 | 0.014 | 0.016 |
| Tylodelphys jenynsiae (0.0–0.9%) | 0.112 | 0.137 | 0.135 | 0.135 | 0.168 | 0.158 | 0.142 | 0.159 | 0.140 | 0.138 | 0.149 | 0.165 | 0.158 | 0.143 | 0.158 | 0.167 | 0.146 | 0.160 | 0.156 | 0.166 | 0.149 | 0.141 | 0.148 | 0.144 | 0.146 | 0.152 | 0.132 | 0.104 | 0.006 | 0.018 | 0.017 | 0.018 | 0.018 | 0.017 | 0.015 | 0.018 | 0.015 | 0.018 | 0.016 | 0.018 |
| Tylodelphys mashonensis (0.0–0.3%) | 0.146 | 0.143 | 0.138 | 0.121 | 0.149 | 0.152 | 0.141 | 0.157 | 0.149 | 0.144 | 0.156 | 0.148 | 0.152 | 0.136 | 0.149 | 0.149 | 0.135 | 0.146 | 0.146 | 0.164 | 0.144 | 0.152 | 0.159 | 0.158 | 0.147 | 0.126 | 0.116 | 0.120 | 0.132 | 0.001 | 0.017 | 0.018 | 0.015 | 0.017 | 0.018 | 0.018 | 0.017 | 0.017 | 0.017 | 0.018 |
| Tylodelphys scheuringi (0.0–1.2%) | 0.129 | 0.135 | 0.134 | 0.120 | 0.158 | 0.159 | 0.145 | 0.158 | 0.132 | 0.141 | 0.136 | 0.148 | 0.146 | 0.138 | 0.156 | 0.165 | 0.131 | 0.144 | 0.146 | 0.167 | 0.152 | 0.146 | 0.155 | 0.145 | 0.118 | 0.140 | 0.129 | 0.118 | 0.116 | 0.126 | 0.005 | 0.018 | 0.018 | 0.014 | 0.017 | 0.017 | 0.018 | 0.014 | 0.015 | 0.018 |
| Tylodelphys sp. 2 LIN1 | 0.144 | 0.147 | 0.156 | 0.147 | 0.183 | 0.165 | 0.133 | 0.168 | 0.161 | 0.144 | 0.152 | 0.170 | 0.174 | 0.143 | 0.165 | 0.183 | 0.153 | 0.183 | 0.171 | 0.186 | 0.163 | 0.162 | 0.171 | 0.162 | 0.161 | 0.134 | 0.114 | 0.127 | 0.120 | 0.124 | 0.126 | ‐ | 0.017 | 0.018 | 0.018 | 0.017 | 0.019 | 0.018 | 0.018 | 0.018 |
| Tylodelphys sp. 2 LIN2 (0.9%) | 0.132 | 0.126 | 0.145 | 0.112 | 0.156 | 0.129 | 0.128 | 0.153 | 0.124 | 0.133 | 0.127 | 0.140 | 0.153 | 0.124 | 0.133 | 0.147 | 0.135 | 0.175 | 0.136 | 0.156 | 0.150 | 0.144 | 0.162 | 0.144 | 0.147 | 0.123 | 0.108 | 0.124 | 0.125 | 0.097 | 0.130 | 0.097 | 0.009 | 0.016 | 0.018 | 0.017 | 0.017 | 0.015 | 0.017 | 0.019 |
| Tylodelphys sp. 3 (0.3–0.9%) | 0.132 | 0.123 | 0.134 | 0.108 | 0.150 | 0.147 | 0.123 | 0.139 | 0.134 | 0.124 | 0.132 | 0.135 | 0.125 | 0.115 | 0.132 | 0.154 | 0.119 | 0.131 | 0.141 | 0.154 | 0.134 | 0.137 | 0.129 | 0.129 | 0.122 | 0.139 | 0.107 | 0.079 | 0.118 | 0.111 | 0.081 | 0.124 | 0.112 | 0.006 | 0.015 | 0.016 | 0.017 | 0.014 | 0.013 | 0.017 |
| Tylodelphys sp. 4 (0.0–0.3%) | 0.136 | 0.146 | 0.143 | 0.119 | 0.153 | 0.144 | 0.121 | 0.148 | 0.139 | 0.124 | 0.140 | 0.160 | 0.142 | 0.127 | 0.134 | 0.143 | 0.128 | 0.159 | 0.145 | 0.150 | 0.157 | 0.139 | 0.131 | 0.138 | 0.128 | 0.133 | 0.131 | 0.108 | 0.101 | 0.130 | 0.122 | 0.141 | 0.127 | 0.099 | 0.004 | 0.018 | 0.014 | 0.017 | 0.016 | 0.017 |
| Tylodelphys sp. 5 (0.3%) | 0.127 | 0.133 | 0.139 | 0.127 | 0.147 | 0.134 | 0.107 | 0.147 | 0.134 | 0.130 | 0.143 | 0.127 | 0.139 | 0.122 | 0.145 | 0.142 | 0.145 | 0.166 | 0.133 | 0.133 | 0.133 | 0.136 | 0.146 | 0.126 | 0.121 | 0.103 | 0.091 | 0.101 | 0.126 | 0.126 | 0.124 | 0.115 | 0.115 | 0.103 | 0.120 | 0.003 | 0.018 | 0.016 | 0.017 | 0.017 |
| Tylodelphys sp. 6 (0.6%) | 0.104 | 0.130 | 0.127 | 0.118 | 0.149 | 0.142 | 0.145 | 0.161 | 0.135 | 0.137 | 0.112 | 0.149 | 0.127 | 0.140 | 0.135 | 0.136 | 0.129 | 0.171 | 0.144 | 0.141 | 0.147 | 0.145 | 0.145 | 0.151 | 0.132 | 0.143 | 0.124 | 0.128 | 0.086 | 0.122 | 0.122 | 0.136 | 0.114 | 0.111 | 0.082 | 0.117 | 0.006 | 0.017 | 0.016 | 0.018 |
| Tylodelphys sp. A*** (0.0–0.9%) | 0.122 | 0.105 | 0.138 | 0.108 | 0.146 | 0.138 | 0.125 | 0.131 | 0.134 | 0.124 | 0.128 | 0.139 | 0.117 | 0.118 | 0.139 | 0.139 | 0.133 | 0.135 | 0.109 | 0.149 | 0.147 | 0.126 | 0.146 | 0.129 | 0.124 | 0.143 | 0.129 | 0.084 | 0.111 | 0.110 | 0.074 | 0.125 | 0.101 | 0.071 | 0.108 | 0.100 | 0.097 | 0.003 | 0.016 | 0.018 |
| Tylodelphy sp. IBC–2016 (0.0–0.6%) | 0.106 | 0.121 | 0.118 | 0.094 | 0.143 | 0.154 | 0.125 | 0.141 | 0.124 | 0.114 | 0.125 | 0.133 | 0.118 | 0.133 | 0.130 | 0.141 | 0.125 | 0.143 | 0.135 | 0.136 | 0.143 | 0.126 | 0.152 | 0.129 | 0.116 | 0.122 | 0.093 | 0.075 | 0.104 | 0.109 | 0.086 | 0.123 | 0.119 | 0.072 | 0.102 | 0.106 | 0.100 | 0.092 | 0.004 | 0.017 |
| Tylodelphys sp. IND (0.3%) | 0.112 | 0.126 | 0.138 | 0.114 | 0.159 | 0.164 | 0.125 | 0.152 | 0.126 | 0.135 | 0.151 | 0.157 | 0.150 | 0.143 | 0.147 | 0.153 | 0.141 | 0.156 | 0.142 | 0.151 | 0.141 | 0.139 | 0.160 | 0.138 | 0.152 | 0.116 | 0.126 | 0.118 | 0.121 | 0.129 | 0.127 | 0.124 | 0.127 | 0.114 | 0.114 | 0.112 | 0.124 | 0.128 | 0.114 | 0.003 |
Table 16.
Average cox1 divergence within and between genera of Diplostomidae-II. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. On the diagonal are the average within group divergence values. Numbers within parentheses after species names represent the range of percent divergence within groups. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 102 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 307 positions in the final dataset
| Alaria sp.1 | Alaria sp.2 | B. damni. | Bolb. sp. | B. sp.BOLD | D.gen.sp.O | D.gen.sp.X | H. triloba | N. americ. | O.scardinii | Orni. sp. 1 | Orni. sp. 2 | Orni. sp. 3 | Orni. sp. 4 | Orni. sp. 8 | P. brevic. | P.cetrarchi | P.cuticola | Post. sp. 1 | Post. sp. 2 | Post. sp. 4 | Post. sp. 5 | Post. sp. 7 | Post. sp. 8 | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Alaria sp. 1 | ‐ | 0.017 | 0.022 | 0.022 | 0.022 | 0.023 | 0.022 | 0.019 | 0.021 | 0.022 | 0.023 | 0.022 | 0.022 | 0.022 | 0.022 | 0.022 | 0.022 | 0.022 | 0.023 | 0.022 | 0.021 | 0.023 | 0.021 | 0.023 |
| Alaria sp. 2 (0.3–1.0%) | 0.109 | 0.007 | 0.022 | 0.022 | 0.023 | 0.023 | 0.023 | 0.019 | 0.021 | 0.024 | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 | 0.023 | 0.022 | 0.023 | 0.022 | 0.022 | 0.024 | 0.023 | 0.022 |
| Bolbophorus damnificus | 0.189 | 0.189 | ‐ | 0.020 | 0.019 | 0.023 | 0.022 | 0.021 | 0.021 | 0.022 | 0.023 | 0.021 | 0.020 | 0.021 | 0.022 | 0.022 | 0.022 | 0.022 | 0.024 | 0.023 | 0.021 | 0.024 | 0.021 | 0.022 |
| Bolbophorus sp. (0.0–3.9%) | 0.202 | 0.210 | 0.156 | 0.012 | 0.020 | 0.022 | 0.022 | 0.022 | 0.022 | 0.022 | 0.023 | 0.021 | 0.021 | 0.021 | 0.022 | 0.022 | 0.022 | 0.022 | 0.023 | 0.022 | 0.020 | 0.023 | 0.021 | 0.023 |
| Bolbophorus sp. BOLD | 0.176 | 0.212 | 0.121 | 0.153 | ‐ | 0.023 | 0.021 | 0.022 | 0.022 | 0.021 | 0.022 | 0.020 | 0.021 | 0.021 | 0.021 | 0.022 | 0.022 | 0.021 | 0.022 | 0.021 | 0.019 | 0.022 | 0.022 | 0.024 |
| Diplostomidae gen. sp. O*** (0.0–1.0%) | 0.213 | 0.221 | 0.203 | 0.193 | 0.199 | 0.003 | 0.018 | 0.022 | 0.021 | 0.018 | 0.019 | 0.016 | 0.016 | 0.018 | 0.018 | 0.021 | 0.022 | 0.021 | 0.021 | 0.021 | 0.019 | 0.020 | 0.021 | 0.021 |
| Diplostomidae gen. sp. X*** | 0.202 | 0.213 | 0.189 | 0.202 | 0.179 | 0.115 | ‐ | 0.022 | 0.022 | 0.018 | 0.018 | 0.014 | 0.015 | 0.017 | 0.018 | 0.020 | 0.021 | 0.021 | 0.021 | 0.020 | 0.018 | 0.020 | 0.021 | 0.022 |
| Hysteromorpha triloba (4.2%) | 0.151 | 0.159 | 0.184 | 0.211 | 0.195 | 0.208 | 0.213 | 0.042 | 0.020 | 0.020 | 0.021 | 0.021 | 0.021 | 0.022 | 0.021 | 0.021 | 0.021 | 0.021 | 0.022 | 0.022 | 0.021 | 0.023 | 0.021 | 0.023 |
| Neodiplostomum americanum (0.3–1.3%) | 0.162 | 0.163 | 0.179 | 0.194 | 0.182 | 0.199 | 0.196 | 0.176 | 0.008 | 0.021 | 0.022 | 0.022 | 0.021 | 0.021 | 0.020 | 0.023 | 0.022 | 0.022 | 0.023 | 0.022 | 0.021 | 0.023 | 0.022 | 0.022 |
| Ornithodiplostomum scardinii | 0.202 | 0.227 | 0.195 | 0.199 | 0.189 | 0.128 | 0.121 | 0.199 | 0.186 | ‐ | 0.019 | 0.017 | 0.017 | 0.019 | 0.019 | 0.021 | 0.021 | 0.021 | 0.022 | 0.021 | 0.020 | 0.021 | 0.020 | 0.023 |
| Ornithodiplostomum sp. 1 (0.3%) | 0.228 | 0.232 | 0.202 | 0.212 | 0.189 | 0.138 | 0.132 | 0.195 | 0.222 | 0.148 | 0.003 | 0.018 | 0.018 | 0.020 | 0.019 | 0.020 | 0.020 | 0.022 | 0.021 | 0.021 | 0.019 | 0.020 | 0.021 | 0.022 |
| Ornithodiplostomum sp. 2 (0.0–3.9%) | 0.207 | 0.229 | 0.174 | 0.191 | 0.161 | 0.105 | 0.082 | 0.203 | 0.200 | 0.113 | 0.128 | 0.023 | 0.012 | 0.017 | 0.016 | 0.018 | 0.020 | 0.020 | 0.021 | 0.020 | 0.017 | 0.019 | 0.019 | 0.021 |
| Ornithodiplostomum sp. 3 (2.0–4.2%) | 0.219 | 0.218 | 0.174 | 0.203 | 0.190 | 0.107 | 0.090 | 0.205 | 0.197 | 0.118 | 0.135 | 0.064 | 0.033 | 0.016 | 0.017 | 0.019 | 0.019 | 0.020 | 0.021 | 0.021 | 0.018 | 0.020 | 0.020 | 0.020 |
| Ornithodiplostomum sp. 4 (0.3–2.9%) | 0.224 | 0.224 | 0.185 | 0.184 | 0.173 | 0.117 | 0.116 | 0.215 | 0.198 | 0.143 | 0.158 | 0.114 | 0.104 | 0.020 | 0.017 | 0.019 | 0.021 | 0.021 | 0.021 | 0.020 | 0.018 | 0.022 | 0.019 | 0.022 |
| Ornithodiplostomum sp. 8 (0.0–3.9%) | 0.212 | 0.227 | 0.196 | 0.196 | 0.186 | 0.127 | 0.129 | 0.201 | 0.172 | 0.128 | 0.148 | 0.113 | 0.117 | 0.125 | 0.013 | 0.021 | 0.020 | 0.020 | 0.020 | 0.019 | 0.017 | 0.020 | 0.020 | 0.021 |
| Posthodiplostomum brevicaudatum (0.3–2.0%) | 0.227 | 0.237 | 0.204 | 0.213 | 0.203 | 0.155 | 0.153 | 0.224 | 0.239 | 0.172 | 0.158 | 0.137 | 0.146 | 0.149 | 0.176 | 0.013 | 0.020 | 0.023 | 0.022 | 0.022 | 0.020 | 0.021 | 0.021 | 0.021 |
| Posthodiplostomum cetrarchi (0.0%) | 0.212 | 0.227 | 0.189 | 0.210 | 0.182 | 0.185 | 0.176 | 0.217 | 0.216 | 0.173 | 0.145 | 0.160 | 0.159 | 0.174 | 0.170 | 0.155 | 0.000 | 0.022 | 0.021 | 0.020 | 0.019 | 0.020 | 0.020 | 0.020 |
| Posthodiplostomum cuticola | 0.205 | 0.205 | 0.195 | 0.196 | 0.182 | 0.185 | 0.182 | 0.182 | 0.213 | 0.186 | 0.191 | 0.173 | 0.178 | 0.185 | 0.171 | 0.227 | 0.179 | ‐ | 0.021 | 0.020 | 0.019 | 0.023 | 0.022 | 0.022 |
| Posthodiplostomum sp. 1 | 0.215 | 0.214 | 0.221 | 0.202 | 0.186 | 0.173 | 0.166 | 0.208 | 0.208 | 0.195 | 0.184 | 0.163 | 0.178 | 0.174 | 0.154 | 0.197 | 0.169 | 0.169 | ‐ | 0.010 | 0.021 | 0.021 | 0.021 | 0.020 |
| Posthodiplostomum sp. 2 | 0.189 | 0.185 | 0.208 | 0.196 | 0.176 | 0.165 | 0.160 | 0.192 | 0.191 | 0.189 | 0.174 | 0.156 | 0.167 | 0.166 | 0.144 | 0.192 | 0.160 | 0.153 | 0.036 | ‐ | 0.020 | 0.023 | 0.022 | 0.022 |
| Posthodiplostomum sp. 4 (1.0–4.6%) | 0.202 | 0.215 | 0.181 | 0.174 | 0.159 | 0.145 | 0.140 | 0.189 | 0.198 | 0.171 | 0.145 | 0.129 | 0.143 | 0.149 | 0.142 | 0.176 | 0.148 | 0.161 | 0.173 | 0.167 | 0.031 | 0.020 | 0.020 | 0.020 |
| Posthodiplostomum sp. 5 | 0.238 | 0.255 | 0.231 | 0.226 | 0.199 | 0.173 | 0.169 | 0.226 | 0.234 | 0.186 | 0.145 | 0.164 | 0.180 | 0.197 | 0.176 | 0.187 | 0.160 | 0.221 | 0.169 | 0.192 | 0.156 | ‐ | 0.021 | 0.022 |
| Posthodiplostomum sp. 7 (0.3–1.0%) | 0.204 | 0.228 | 0.181 | 0.197 | 0.195 | 0.182 | 0.164 | 0.194 | 0.203 | 0.175 | 0.189 | 0.162 | 0.173 | 0.151 | 0.167 | 0.188 | 0.182 | 0.201 | 0.177 | 0.190 | 0.179 | 0.189 | 0.007 | 0.021 |
| Posthodiplostomum sp. 8 (0.3–0.7%) | 0.231 | 0.213 | 0.192 | 0.199 | 0.228 | 0.189 | 0.191 | 0.226 | 0.208 | 0.208 | 0.194 | 0.182 | 0.169 | 0.182 | 0.170 | 0.192 | 0.168 | 0.199 | 0.164 | 0.177 | 0.159 | 0.194 | 0.183 | 0.004 |
Table 17.
Average cox1 divergence within and between groups of Strigeidae-I. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. Average intraspecific divergence values are in bold and lie on the diagonal. The range of intraspecific values are given as percentages next to species names. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 152 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 345 positions in the final dataset
| C. cornut. | C. flabell. | C. marcog. | C. sp. A | C. sp. B | C. sp. C | C. sp. D | C. sp. E | C. sp. F | C. sp. ‘lutzi’ | C. strigeo. | Ca. medio. | Ca. sp. | Ic. pileatus | Ic. sp. 2 | Ic. sp. 3 | T. sheurin. | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Cotylurus cornutus (0.0–2.9%) | 0.011 | 0.010 | 0.013 | 0.018 | 0.017 | 0.012 | 0.014 | 0.013 | 0.010 | 0.016 | 0.015 | 0.020 | 0.020 | 0.019 | 0.019 | 0.018 | 0.021 |
| C. flabelliformis (0.3%) | 0.042 | 0.003 | 0.014 | 0.019 | 0.017 | 0.013 | 0.015 | 0.013 | 0.011 | 0.016 | 0.016 | 0.020 | 0.020 | 0.019 | 0.019 | 0.019 | 0.021 |
| C. marcogliesei (0.0–1.2%) | 0.070 | 0.073 | 0.005 | 0.018 | 0.016 | 0.013 | 0.015 | 0.013 | 0.012 | 0.016 | 0.015 | 0.021 | 0.020 | 0.020 | 0.019 | 0.018 | 0.021 |
| Cotylurus sp. A (0.0–1.4%) | 0.132 | 0.133 | 0.134 | 0.003 | 0.019 | 0.019 | 0.018 | 0.019 | 0.019 | 0.021 | 0.019 | 0.020 | 0.020 | 0.020 | 0.019 | 0.018 | 0.020 |
| Cotylurus sp. B | 0.127 | 0.123 | 0.112 | 0.136 | ‐ | 0.017 | 0.018 | 0.017 | 0.017 | 0.019 | 0.018 | 0.020 | 0.020 | 0.020 | 0.019 | 0.019 | 0.021 |
| Cotylurus sp. C (0.0%) | 0.064 | 0.064 | 0.071 | 0.147 | 0.116 | 0.000 | 0.014 | 0.014 | 0.014 | 0.016 | 0.015 | 0.020 | 0.020 | 0.020 | 0.019 | 0.019 | 0.021 |
| Cotylurus sp. D | 0.084 | 0.084 | 0.085 | 0.130 | 0.136 | 0.081 | ‐ | 0.014 | 0.015 | 0.016 | 0.013 | 0.019 | 0.020 | 0.020 | 0.019 | 0.019 | 0.022 |
| Cotylurus sp. E (0.0–0.6%) | 0.074 | 0.069 | 0.068 | 0.142 | 0.118 | 0.077 | 0.077 | 0.002 | 0.013 | 0.015 | 0.014 | 0.021 | 0.021 | 0.018 | 0.017 | 0.019 | 0.021 |
| Cotylurus sp. F (0.0–0.9%) | 0.044 | 0.043 | 0.057 | 0.140 | 0.117 | 0.074 | 0.090 | 0.062 | 0.004 | 0.017 | 0.016 | 0.020 | 0.021 | 0.019 | 0.020 | 0.019 | 0.021 |
| Cotylurus sp. ‘lutzi’ | 0.111 | 0.100 | 0.114 | 0.173 | 0.151 | 0.107 | 0.101 | 0.104 | 0.122 | ‐ | 0.016 | 0.020 | 0.020 | 0.019 | 0.019 | 0.018 | 0.021 |
| C. strigeoides (0.0–1.7%) | 0.096 | 0.100 | 0.085 | 0.145 | 0.139 | 0.097 | 0.069 | 0.078 | 0.098 | 0.114 | 0.007 | 0.021 | 0.021 | 0.019 | 0.019 | 0.019 | 0.021 |
| Cardiocephaloides medioconiger (0.0%) | 0.167 | 0.159 | 0.186 | 0.174 | 0.168 | 0.168 | 0.154 | 0.181 | 0.175 | 0.165 | 0.185 | 0.000 | 0.015 | 0.019 | 0.019 | 0.018 | 0.020 |
| Cardiocephaloides sp. | 0.173 | 0.174 | 0.168 | 0.171 | 0.159 | 0.174 | 0.174 | 0.180 | 0.181 | 0.174 | 0.182 | 0.090 | ‐ | 0.020 | 0.018 | 0.018 | 0.021 |
| Ichthyocotylurus pileatus | 0.151 | 0.154 | 0.166 | 0.161 | 0.164 | 0.170 | 0.158 | 0.142 | 0.156 | 0.156 | 0.154 | 0.156 | 0.179 | 0.002 | 0.015 | 0.015 | 0.020 |
| Ichthyocotylurus sp. 2 | 0.147 | 0.148 | 0.143 | 0.145 | 0.136 | 0.142 | 0.148 | 0.117 | 0.160 | 0.157 | 0.142 | 0.151 | 0.145 | 0.092 | ‐ | 0.014 | 0.020 |
| Ichthyocotylurus sp. 3 | 0.134 | 0.142 | 0.132 | 0.142 | 0.145 | 0.142 | 0.142 | 0.140 | 0.140 | 0.142 | 0.146 | 0.142 | 0.148 | 0.095 | 0.078 | ‐ | 0.018 |
| Tylodelphys sheuringi (out) | 0.200 | 0.194 | 0.190 | 0.177 | 0.194 | 0.200 | 0.206 | 0.195 | 0.204 | 0.191 | 0.209 | 0.191 | 0.186 | 0.175 | 0.171 | 0.139 | ‐ |
Table 18.
Average cox1 divergence within and between groups of Strigeidae-II. The number of base differences per site from averaging over all sequence pairs between groups are shown. Standard error estimate(s) are shown above the diagonal. Average intraspecific divergence values lie on the diagonal. The range of intraspecific values are given as percentages next to species names. Values in red are above the delineation cut‐off. The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). The analysis involved 309 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. There were a total of 377 positions in the final dataset
| A. jamies. | A. sp. 1 | A. sp. 1x | A. sp. 3 | A. sp. 4 | A. sp. A | A. sp. B | A. sp. C | Au. b. LIN1 | Au. mclaugh. | Au. niew. | Au. LIN10 | Au. LIN2 | Au. LIN3 | Au. LIN4 | Au. LIN5 | Au. LIN6 | Au. LIN8 | Au. LIN9A | Au. LIN9B | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Apatemon sp. ‘jamiesoni’ (0.3%) | 0.003 | 0.015 | 0.014 | 0.015 | 0.016 | 0.016 | 0.015 | 0.014 | 0.018 | 0.018 | 0.017 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.018 | 0.018 | 0.017 | 0.018 |
| Apatemon sp. 1 (0.8%) | 0.103 | 0.008 | 0.009 | 0.014 | 0.015 | 0.014 | 0.013 | 0.015 | 0.018 | 0.017 | 0.018 | 0.017 | 0.019 | 0.019 | 0.018 | 0.017 | 0.018 | 0.017 | 0.017 | 0.018 |
| Apatemon sp. 1x (0.5%) | 0.101 | 0.038 | 0.005 | 0.014 | 0.015 | 0.014 | 0.014 | 0.014 | 0.017 | 0.017 | 0.017 | 0.016 | 0.019 | 0.018 | 0.017 | 0.018 | 0.017 | 0.017 | 0.017 | 0.017 |
| Apatemon sp. 3 (0.0%) | 0.097 | 0.092 | 0.085 | 0.000 | 0.015 | 0.016 | 0.015 | 0.015 | 0.017 | 0.018 | 0.017 | 0.017 | 0.019 | 0.017 | 0.017 | 0.018 | 0.017 | 0.016 | 0.016 | 0.017 |
| Apatemon sp. 4 (0.3%) | 0.118 | 0.095 | 0.090 | 0.094 | 0.003 | 0.018 | 0.016 | 0.016 | 0.018 | 0.018 | 0.017 | 0.017 | 0.019 | 0.019 | 0.017 | 0.019 | 0.017 | 0.017 | 0.018 | 0.019 |
| Apatemon sp. A ***(0.0–1.0%) | 0.124 | 0.094 | 0.087 | 0.114 | 0.131 | 0.004 | 0.012 | 0.015 | 0.019 | 0.019 | 0.019 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.018 | 0.018 | 0.018 | 0.018 |
| Apatemon sp. B*** | 0.113 | 0.084 | 0.085 | 0.093 | 0.107 | 0.058 | ‐ | 0.015 | 0.018 | 0.019 | 0.018 | 0.018 | 0.019 | 0.017 | 0.018 | 0.019 | 0.018 | 0.017 | 0.017 | 0.018 |
| Apatemon sp. C ***(0.0–0.3%) | 0.097 | 0.091 | 0.092 | 0.093 | 0.099 | 0.101 | 0.092 | 0.001 | 0.017 | 0.018 | 0.017 | 0.017 | 0.018 | 0.017 | 0.017 | 0.018 | 0.017 | 0.017 | 0.016 | 0.016 |
| Australapatemon burti LIN1 (0.0–6.4%) | 0.147 | 0.138 | 0.136 | 0.131 | 0.142 | 0.158 | 0.149 | 0.126 | 0.011 | 0.014 | 0.016 | 0.013 | 0.012 | 0.014 | 0.013 | 0.015 | 0.013 | 0.015 | 0.015 | 0.015 |
| Australapatemon mclaughlini (0.0–0.5%) | 0.150 | 0.140 | 0.133 | 0.142 | 0.156 | 0.165 | 0.162 | 0.148 | 0.097 | 0.002 | 0.017 | 0.011 | 0.014 | 0.015 | 0.014 | 0.015 | 0.012 | 0.017 | 0.015 | 0.015 |
| Australapatemon niewiadomski (0.0–2.1%) | 0.146 | 0.154 | 0.138 | 0.145 | 0.145 | 0.156 | 0.157 | 0.146 | 0.128 | 0.142 | 0.013 | 0.017 | 0.017 | 0.017 | 0.017 | 0.018 | 0.017 | 0.017 | 0.017 | 0.017 |
| Australapatemon sp. LIN10*** | 0.139 | 0.134 | 0.117 | 0.127 | 0.139 | 0.142 | 0.143 | 0.129 | 0.084 | 0.050 | 0.130 | ‐ | 0.015 | 0.015 | 0.013 | 0.014 | 0.010 | 0.016 | 0.015 | 0.015 |
| Australapatemon sp. LIN2 | 0.158 | 0.155 | 0.149 | 0.159 | 0.153 | 0.170 | 0.159 | 0.148 | 0.075 | 0.085 | 0.140 | 0.093 | ‐ | 0.014 | 0.014 | 0.017 | 0.014 | 0.015 | 0.015 | 0.015 |
| Australapatemon sp. LIN3 | 0.158 | 0.160 | 0.154 | 0.133 | 0.150 | 0.156 | 0.141 | 0.135 | 0.087 | 0.109 | 0.132 | 0.098 | 0.088 | ‐ | 0.015 | 0.016 | 0.014 | 0.016 | 0.016 | 0.015 |
| Australapatemon sp. LIN4 (0.3–4.8%) | 0.161 | 0.158 | 0.149 | 0.139 | 0.148 | 0.154 | 0.163 | 0.151 | 0.093 | 0.101 | 0.134 | 0.086 | 0.098 | 0.104 | 0.026 | 0.015 | 0.012 | 0.014 | 0.015 | 0.015 |
| Australapatemon sp. LIN5 | 0.174 | 0.145 | 0.146 | 0.143 | 0.167 | 0.172 | 0.167 | 0.145 | 0.113 | 0.099 | 0.144 | 0.077 | 0.138 | 0.119 | 0.117 | ‐ | 0.015 | 0.017 | 0.016 | 0.016 |
| Australapatemon sp. LIN6 (0.0–4.2%) | 0.144 | 0.146 | 0.129 | 0.135 | 0.134 | 0.154 | 0.151 | 0.138 | 0.086 | 0.067 | 0.137 | 0.045 | 0.094 | 0.105 | 0.081 | 0.097 | 0.017 | 0.015 | 0.015 | 0.014 |
| Australapatemon sp. LIN8 (0.0–1.0%) | 0.143 | 0.140 | 0.136 | 0.120 | 0.136 | 0.147 | 0.139 | 0.140 | 0.100 | 0.124 | 0.136 | 0.107 | 0.112 | 0.117 | 0.105 | 0.147 | 0.109 | 0.002 | 0.014 | 0.015 |
| Australapatemon sp. LIN9A (0.0–3.2%) | 0.141 | 0.136 | 0.130 | 0.116 | 0.146 | 0.142 | 0.132 | 0.125 | 0.104 | 0.112 | 0.136 | 0.099 | 0.097 | 0.117 | 0.115 | 0.127 | 0.107 | 0.088 | 0.009 | 0.011 |
| Australapatemon sp. LIN9B (0.3–1.1%) | 0.145 | 0.145 | 0.133 | 0.123 | 0.149 | 0.141 | 0.141 | 0.111 | 0.102 | 0.111 | 0.140 | 0.097 | 0.100 | 0.100 | 0.117 | 0.117 | 0.105 | 0.101 | 0.061 | 0.007 |
Table 19.
Digenean trematode diversity of Alberta. A review of the literature is supplemented with species records gathered from this study and previous molecular studies to account for the known trematodes of Alberta, Canada. Host and location records are provided herein
| Family | Trematode Species | Life Cycle Stage | Locations | Snail Host Species | Definitive /Other Host | GenBank Accession Number(s) | Reference |
|---|---|---|---|---|---|---|---|
| Allocreadiidae | Crepidostomum farionis | Adult | Cold Lake (54.30'N, 110W) | Unidentified | Cisco, Whitefish, Coho Salmon | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | |
| Adult | Caribou Lake, Eva Lake, Fleming Lake, Margaret Lake, Pitchimi Lake, Semo Lake, Sucker Lake, Wentzel Lake | Unidentified | Various fish species | Baldwin, R.E. and Goater, C.P., 2003, JP, 89(2):215‐225 | |||
| Crepidostomum isotomum | Adult | Garner Lake, Alberta | Unidentified | Yellow Perch | Zelmer, D.A. and Arai, H.P., 1998, JP, 84(1):24.28 | ||
| Bolbophoridae | Bolbophorus sp. | Cercaria | Canada: Alberta, Buffalo Lake | Helisoma trivolvis | Unidentified | KT831373 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. |
| Cercaria | Canada: Alberta, Buffalo Lake, Isle Lake, Wabamun Lake | Helisoma trivolvis | Unidentified | MH368843, MH368847, MH368850, MH368862, MH368871, MH368892, MH368918, MH368919 | Present study | ||
| Bunoderidae | Bunodera luciopercae | Adult | Cold Lake (54.30'N, 110W) | Unidentified | Unidentified | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | |
| Diplostomidae | Diplostomidae gen. sp. O | Cercaria | Canada: Alberta, Buffalo Lake | Physa gyrina | Unidentified | KT831363§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. |
| Cercaria | Canada: Alberta, Buffalo Lake, Wabamun Lake, Gull Lake, Isle Lake | Physa gyrina | Unidentified | MH368825, MH368851, MH368854, MH368855, MH368879, MH368880, MH368881, MH368882, MH368883, MH368884, MH368885, MH368886, MH368887, MH368888, MH368889, MH368890, MH368893, MH368903, MH368904, MH368905, MH368906, MH368915, MH368916, MH368917, MH368934, MH368935, MH368936, MH368937, MH368938, MH368939, MH368940, MH368941, MH368942 | Present study | ||
| Diplostomidae gen. sp. X | Cercaria | Canada: Alberta, Isle Lake | Physa gyrina | Unidentified | MH368907 | Present study | |
| Diplostomum adamsi | Metacercaria | Garner Lake, Alberta | Unidentified | Yellow Perch | Zelmer, D.A. and Arai, H.P., 1998, JP, 84(1):24.28 | ||
| Diplostomum baeri bucculentum | Metacercaria | NW Territories | Unidentified | Least Cisco | Shostak, et al, 1987, Can. J. Zool., 65 | ||
| Diplostomum baeri LIN2 | Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake | Stagnicola elodes | Unidentified | MH368863, MH368874, MH368875, MH368928 | Present study | |
| Diplostomum indistinctum | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KT831379 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Diplostomum sp. 1 | Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake | Stagnicola elodes | Unidentified | MH368857, MH368896, MH368932, MH368943, MH368945 | Present study | |
| Diplostomum sp. 2 | unknown | Margaret Lake, AB | Unidentified | Trout Perch | Baldwin, R.E. and Goater, C.P., 2003, JP, 89(2):215‐225 | ||
| Diplostomum sp. 3 | Cercaria | Canada: Alberta, Wabamun Lake | Lymnaea stagnalis | Unidentified | KT831358 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Wabamun Lake | Lymnaea stagnalis | Unidentified | MH368837, MH368858 | Present study | ||
| Diplostomum sp. 4 | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | KT831354 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake, Gull Lake, Buffalo Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH368808, MH368809, MH368813, MH368814, MH368815, MH368816, MH368818, MH368819, MH368820, MH368821, MH368822, MH368823, MH368824, MH368826, MH368827, MH368828, MH368829, MH368830, MH368831, MH368832, MH368833, MH368834, MH368835, MH368836, MH368838, MH368839, MH368840, MH368841, MH368844, MH368845, MH368846, MH368848, MH368849, MH368853, MH368856, MH368859, MH368860, MH368861, MH368864, MH368865, MH368866, MH368867, MH368868, MH368869, MH368870, MH368872, MH368873, MH368876, MH368877, MH368891, MH368898, MH368899, MH368900, MH368901, MH368911, MH368913, MH368914, MH368924, MH368925, MH368926, MH368927, MH368929, MH368930, MH368931, MH368944, MH368946, MH368947, MH368948, MH368949, MH368950 | Present study | ||
| Diplostomum sp. A | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH368817 | Present study | |
| Diplostomum sp. B | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH368933 | Present study | |
| Diplostomum sp. C | Cercaria | Canada: Alberta, Gull Lake, Wabamun Lake, Isle Lake | Stagnicola elodes | Unidentified | KT831360§, KT831378§, KT831382§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Gull Lake, Wabamun Lake, Isle Lake | Stagnicola elodes, Helisoma trivolvis (MGC208) | Unidentified | MH368810, MH368811, MH368812, MH368852, MH368895, MH368902, MH368921, MH368922, MH368923 | Present study | ||
| Diplostomum spathaceum | Adult | Cooking Lake | Unidentified | Bonaparte's Gulls | Hair, J.D. and Holmes, J.C., 1970, Can. J. Zool. 48:1129‐1131 | ||
| Larval | Cold Lake (54.30'N, 110W) | Unidentified | Whitefish, Lake Trout, 9‐spine stickleback | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | |||
| Larval | Big Fish Lake, Caribou Lake, Margaret Lake, Wentzel Lake | Unidentified | Various fish species | Baldwin, R.E. and Goater, C.P., 2003, JP, 89(2):215‐225 | |||
| Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | California Gull, Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | |||
| Neodiplostomum americanum | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | KT831357§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Ornithodiplostomum ptychocheilus | Cercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | ||
| Cercaria/Metacercaria | Central Alberta unnamed lake (54.22'N, 113.27'W) | Physa gyrina | Fathead minnows, chickens(experimental) | Schleppe, J.L. and Goater, C.P., 2004, JP, 90(6):1387‐1390 | |||
| Ornithodiplostomum sp. 2 | Cercaria | Canada: Alberta, Wabamun Lake | Physa gyrina | Unidentified | KT831368 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Wabamun Lake | Physa gyrina | Unidentified | KT831368 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Ornithodiplostomum sp. 8 | Cercaria | Canada: Alberta, Pigeon Lake | Physa gyrina | Unidentified | KT831383 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Isle Lake | Physa gyrina | Unidentified | MH368908, MH368910, MH368920 | Present study | ||
| Posthodiplostomum minimum | Cercaria/Metacercaria | Central Alberta unnamed lake (54.22'N, 113.27'W) | Physa gyrina | Fathead minnows, chickens(experimental) | Schleppe, J.L. and Goater, C.P., 2004, JP, 90(6):1387‐1390 | ||
| Posthodiplostomum sp. 4 | Cercaria | Canada: Alberta, Isle Lake | Physa gyrina | Unidentified | MH368909, MH368912 | Present study | |
| Tylodelphys podicipina | Adult | 9 lakes in Alberta | Unidentified | Aechmophorus occidentalis, Podiceps grisegena, Podiceps nigricollis | Stock, T.M. and Holmes, J.C., 1988, JP, 74(2): 214‐227 | ||
| Tylodelphys scheuringi | Metacercaria | Garner Lake, Alberta | Unidentified | Yellow perch | Zelmer, D.A. and Arai, H.P., 1998, JP, 84(1):24.28 | ||
| Tylodelphys sp. A | Cercaria | Canada: Alberta, Wabamun Lake | Helisoma trivolvis | Unidentified | KT831356§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Wabamun Lake | Helisoma trivolvis | Unidentified | MH368842, MH368878, MH368894, MH368897 | Present study | ||
| Echinostomatidae | Drepanocephalus spathans | Cercaria | Canada: Alberta, Isle Lake, Buffalo Lake | Helisoma trivolvis | Unidentified | MH368951, MH368952, MH369294 | Present study |
| Cercaria | Canada: Alberta, Buffalo Lake | Helisoma trivolvis | Unidentified | KT831381 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Echinoparyphium recurvatum | Cercaria/Metacercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | ||
| Redia | Isolated pond near Clyde, AB (54.09'N, 113.39'W) | Helisoma trivolvis | Unidentified | Morris and Boag, 1982, Can. J. Zool. | |||
| Adult | 13 Lakes in Alberta | Unidentified | Lesser Scaup | Bush, A.O. and Holmes, J.C., 1986, Can. J. Zool. 64:132‐141 | |||
| Adult | Alberta | Unidentified | Great horned owls | Ramalingam, S. and Samuel, W.M., 1978, Can. J. Zool. 56:2454‐2456 | |||
| Echinoparyphium recurvatum, flexum | Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | California Gull, Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | ||
| Echinoparyphium sp. 1A | Cercaria | Canada: Alberta, Lac La Nonne, Wabamun Lake, Isle Lake | Physa gyrina, Stagnicola elodes (MGC1954, MGC2104), Helisoma trivolvis (MGC2090) | Unidentified | MH368998, MH368999, MH369001, MH369002, MH369003, MH369004, MH369005, MH369006, MH369007, MH369008, MH369009, MH369010, MH369012, MH369013, MH369014, MH369015, MH369016, MH369017, MH369018, MH369019, MH369022, MH369023, MH369024, MH369025, MH369026, MH369028, MH369031, MH369032, MH369033, MH369034, MH369038, MH369042, MH369044, MH369045, MH369046, MH369047, MH369048, MH369049, MH369052, MH369053, MH369054, MH369055, MH369056, MH369059, MH369060, MH369062, MH369063, MH369065, MH369066, MH369068, MH369070, MH369075, MH369076, MH369087, MH369089, MH369090, MH369091, MH369093, MH369094, MH369095, MH369096, MH369097, MH369098, MH369099, MH369100, MH369101, MH369102, MH369121, MH369122, MH369123, MH369125, MH369131, MH369132, MH369133, MH369136, MH369147, MH369155, MH369156, MH369162, MH369163, MH369164, MH369165, MH369166, MH369167, MH369168, MH369178, MH369188, MH369191 | Present study | |
| Cercaria | Canada: Alberta, Lac La Nonne | Physa gyrina | Unidentified | KT831361§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Echinoparyphium sp. 1B | Cercaria | Canada: Alberta, Isle Lake | Physa gyrina | Unidentified | MH369181 | Present study | |
| Echinoparyphium sp. A | Cercaria | Canada: Alberta, Buffalo Lake, Wabamun Lake, Isle Lake, Lac La Nonne, Gull Lake, Pigeon Lake | Physa gyrina, Stagnicola elodes (MGC1932) | Unidentified | MH369011, MH369035, MH369043, MH369051, MH369058, MH369061, MH369064, MH369069, MH369081, MH369082, MH369083, MH369084, MH369085, MH369113, MH369120, MH369128, MH369161, MH369169, MH369170, MH369171, MH369172, MH369173, MH369174, MH369175, MH369176, MH369177, MH369179, MH369180, MH369182, MH369183, MH369184, MH369185, MH369187 | Present study | |
| Echinoparyphium sp. A2 | Cercaria | Canada: Alberta, Gull Lake | Physa gyrina | Unidentified | MH369190, MH369127 | Present study | |
| Cercaria | Canada: Alberta, Lac La Nonne | Stagnicola elodes | Unidentified | KT831367§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Echinoparyphium sp. B | Cercaria | Canada: Alberta, Lac La Nonne | Stagnicola elodes | Unidentified | MH368969, MH368970, MH368971, MH368987, MH368988, MH369041, MH369074, MH369086, MH369092 | Present study | |
| Echinoparyphium sp. C | Cercaria | Canada: Alberta, Gull Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369088, MH369152 | Present study | |
| Echinoparyphium sp. D | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369189 | Present study | |
| Echinoparyphium sp. E | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes, Lymnaea stagnalis (MGC1878) | Unidentified | MH369109, MH369129, MH369134, MH369135, MH369159 | Present study | |
| Echinoparyphium sp. Lineage 2 | Cercaria | Canada: Alberta, Gull Lake, Isle Lake, Buffalo Lake, Wabamun Lake, Lac La Nonne | Stagnicola elodea, Lymnaea stagnalis (MGC16A/B, MGC369), Helisoma trivolvis (MGC219) | Unidentified | MH368953, MH368954, MH368955, MH368956, MH368957, MH368959, MH368960, MH368961, MH368962, MH368963, MH368964, MH368965, MH368966, MH368967, MH368968, MH368972, MH368973, MH368974, MH368975, MH368976, MH368977, MH368978, MH368979, MH368980, MH368981, MH368982, MH368983, MH368984, MH368985, MH368986, MH368989, MH368990, MH368991, MH368992, MH368993, MH368994, MH368995, MH368996, MH368997, MH369000, MH369021, MH369027, MH369029, MH369036, MH369037, MH369039, MH369050, MH369057, MH369067, MH369071, MH369072, MH369073, MH369077, MH369078, MH369079, MH369103, MH369104, MH369105, MH369106, MH369107, MH369111, MH369112, MH369114, MH369115, MH369116, MH369117, MH369118, MH369119, MH369124, MH369126, MH369137, MH369138, MH369139, MH369140, MH369141, MH369142, MH369143, MH369144, MH369146, MH369148, MH369149, MH369150, MH369151, MH369153, MH369154, MH369160, MH369186 | Present study | |
| Cercaria | Canada: Alberta, Lac La Nonne | Stagnicola elodes | Unidentified | KT831350§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Echinoparyphium sp. Lineage 4 | Cercaria | Canada: Alberta, Wabamun Lake, Buffalo Lake | Helisoma trivolvis | Unidentified | MH369130, MH369158 | Present study | |
| Echinostoma revolutum | Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | California Gull, Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | ||
| Adult | Alberta | Unidentified | Great horned owls | Ramalingam, S. and Samuel, W.M., 1978, Can. J. Zool. 56:2454‐2456 | |||
| Echinostoma revolutum Lineage B | Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake, Wabamun Lake, Isle Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369227, MH369229, MH369230, MH369231, MH369235, MH369242, MH369248, MH369268, MH369279, MH369281, MH369284, MH369286, MH369287, MH369292 | Present study | |
| Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake, Wabamun Lake, Isle Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369192, MH369193, MH369194, MH369195, MH369196, MH369197, MH369200, MH369201, MH369202, MH369204, MH369206, MH369207, MH369208, MH369209, MH369210, MH369211, MH369213, MH369214, MH369215, MH369216, MH369217, MH369218, MH369219, MH369220, MH369221, MH369222 | Present study | ||
| Echinostoma trivolvis Lineage A | Cercaria | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne | Helisoma trivolvis | Unidentified | MH369271 | Present study | |
| Echinostomatidae gen. sp. | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369269, MH369295, MH369297 | Present study | |
| Hypoderaeum sp. Lineage 1 | Cercaria | Canada: Alberta, Gull Lake, Lac La Nonne, Wabamun Lake, Isle Lake | Stagnicola elodes | Unidentified | MH368958, MH369040, MH369108, MH369110, MH369145, MH369157 | Present study | |
| Hypoderaeum sp. Lineage 2 | Cercaria | Canada: Alberta, Isle Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369020, MH369030, MH369080 | Present study | |
| Neopetasiger islandicus | Cercaria | Canada: Alberta, Wabamun Lake | Planorbula armigera | Unidentified | KT831342 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Petasiger nitidius | Cercaria | Amisk Lake (54.35'N, 112.37'W) Baptiste Lake (54.45'N, 113.33'W) | Heliosoma trivolvis | Unidentified | Shostak, A.W., 1992, Can. J. Zool. 71:431‐434 | ||
| Adult | 9 lakes in Alberta | Unidentified | Aechmophorus occidentalis, Podiceps grisegena, Podiceps nigricollis, Podiceps auritus | Stock, T.M. and Holmes, J.C., 1988, JP, 74(2): 214‐227 | |||
| Neopetasiger sp. 4 | Cercaria | Canada: Alberta, Wabamun Lake | Helisoma trivolvis | Unidentified | KT831343, KT831345 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake, Buffalo Lake | Helisoma trivolvis | Unidentified | MH369311, MH369312, MH369313, MH369314, MH369315, MH369316, MH369317, MH369318 | Present study | ||
| Fasciolidae | Fasciola hepatica | Adult | Rimbey, Alberta | Unidentified | Cattle (Holstein steers) | Giebelhaus, I.T. 1998, Can. Vet. J. 39:433 | |
| Fascioloides magna | Adult | Banff National Park (51.12'N, 115.35'W) | Unidentified | Cervus elaphus canadensis | Kralova‐Hromadova, et al., 2010, IJP, 41:373‐383 | ||
| Adult | Cypress Hills, Elk Island and other parts of Alberta | Unidentified | Moose | Samuel, W.M., 1976, Can J Zool, 54(3) | |||
| Gorgoderidae | Gorgoderina simplex | Adult | Eastern Alberta (50.35’‐56.44'N, 110.40’‐114.05'W) | Unidentified | Bufo hemiophrys (Canadian Toad) | Bursey, C.R. and Goldberg, S.R. 1998, JP, 84(3):617‐618 | |
| Phyllodistomum coregoni | Adult | Cold Lake (54.30'N, 110W) | Unidentified | Whitefish | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | ||
| Haematoloechidae | Haematoloechidae gen. sp. A | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | KT831372§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. |
| Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369319, MH369320, MH369321 | Present study | ||
| Lissorchiidae | Lissorchis attenuatum | Adult | Cold Lake (54.30'N, 110W) | Unidentified | 9‐spine stickleback | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | |
| Notocotylidae | Notocotylus sp. A | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KT831348§, KT831364 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. |
| Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake, Gull Lake, Buffalo Lake, Lac La Nonne | Physa gyrina, Stagnicola elodes | Unidentified | MH369326, MH369333, MH369334, MH369335, MH369345, MH369346, MH369349, MH369350, MH369352, MH369411, MH369353, MH369354, MH369355, MH369362, MH369363, MH369364, MH369365, MH369366, MH369367, MH369372, MH369373, MH369378, MH369381, MH369382, MH369383, MH369415, MH369384, MH369387, MH369390, MH369391, MH369417, MH369393, MH369395, MH369396, MH369397, MH369398, MH369400, MH369401, MH369402 | Present study | ||
| Notocotylus sp. B | Cercaria | Canada: Alberta, Wabamun Lake | Physa gyrina | Unidentified | MH369416 | Present study | |
| Notocotylus sp. C | Cercaria | Canada: Alberta, Lac La Nonne | Helisoma trivolvis | Unidentified | MH369356 | Present study | |
| Notocotylus sp. D | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KT831348§ | Gordy, M.A., et al., 2016, Parasitol. Res. | |
| Cercaria | Canada: Alberta, Isle Lake, Gull Lake, Buffalo Lake, Lac La Nonne | Stagnicola elodes, Physa gyrina | Unidentified | MH369386, MH369389, MH369392, MH369399, MH369323, MH369405, MH369324, MH369406, MH369325, MH369327, MH369407, MH369408, MH369328, MH369409, MH369329, MH369330, MH369331, MH369332, MH369336, MH369337, MH369338, MH369339, MH369340, MH369341, MH369342, MH369343, MH369344, MH369410, MH369347, MH369348, MH369351, MH369357, MH369358, MH369359, MH369360, MH369361, MH369368, MH369412, MH369369, MH369370, MH369371, MH369374, MH369375, MH369376, MH369413, MH369414, MH369379, MH369380, MH369385, MH369388, MH369394, MH369403, MH369404 | Present study | ||
| Notocotylus attenuatus | Adult | Breeding resident in Alberta, but found in SW Texas | Unidentified | Green‐winged Teal | Canaris, A.G., Mena, A.C. and Bristol, J.R., 1981, J. Wildlife Dis. 17(1) | ||
| Adult | Alberta | Unidentified | Great horned owls | Ramalingam, S. and Samuel, W.M., 1978, Can. J. Zool. 56:2454‐2456 | |||
| Notocotylus urbanensis | Cercaria/Metacercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | ||
| Paramphistomatidae | Zygocotyle lunata | Cercaria/Metacercaria | Lyle Lake (55.12'N, 112.29W) Beaver impoundment near Fort McMurray (56.31'N, 111.19'W) | Heliosoma trivolvis | CD1 Mice (experimental) | Shostak, A.W., Dharampaul, S., and Belosevic, M., 1993, J. Parasitol. 79(6):922‐929 | |
| Plagiorchiidae | Plagiorchis elegans | Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | California Gull, Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | |
| Plagiorchis sp. | Adult | Alberta | Unidentified | Great horned owls | Ramalingam, S. and Samuel, W.M., 1978, Can. J. Zool. 56:2454‐2456 | ||
| Plagiorchis sp. Lineage 1 | Cercaria | Canada: Alberta, Gull Lake, Lac La Nonne, Buffalo Lake | Stagnicola elodes | Unidentified | MH369420, MH369421, MH369422, MH369433, MH369434, MH369435, MH369441, MH369460, MH369461, MH369463, MH369464 | Present study | |
| Plagiorchis sp. Lineage 2 | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369467 | Present study | |
| Plagiorchis sp. Lineage 3 | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369442, MH369454, MH369466 | Present study | |
| Plagiorchis sp. Lineage 4 | Cercaria | Canada: Alberta, Gull Lake, Lac La Nonne, Buffalo Lake, Wabamun Lake, Isle Lake | Stagnicola elodes | Unidentified | MH369418, MH369423, MH369425, MH369428, MH369429, MH369431, MH369432, MH369436, MH369437, MH369440, MH369447, MH369452, MH369453, MH369456, MH369462, MH369471 | Present study | |
| Plagiorchis sp. Lineage 5 | Cercaria | Canada: Alberta, Gull Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369419, MH369426, MH369427 | Present study | |
| Plagiorchis sp. Lineage 6 | Cercaria | Canada: Alberta, Buffalo Lake | Helisoma trivolvis | Unidentified | MH369470 | Present study | |
| Plagiorchis sp. Lineage 7 | Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake | Lymnaea stagnalis | Unidentified | MH369438, MH369448, MH369455, MH369458, MH369468, MH369469 | Present study | |
| Plagiorchis sp. Lineage 8 | Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake | Stagnicola elodes | Unidentified | MH369449, MH369450, MH369451, MH369459, MH369465 | Present study | |
| Plagiorchis sp. Lineage 9 | Cercaria | Canada: Alberta, Lac La Nonne, Buffalo Lake | Stagnicola elodes | Unidentified | MH369424, MH369430, MH369439, MH369443, MH369444, MH369445, MH369446 | Present study | |
| Psilostomidae | Psilostomidae gen. sp. A | Cercaria | Canada: Alberta, Wabamun Lake | Helisoma trivolvis | Unidentified | MH369477§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. |
| Cercaria | Canada: Alberta, Wabamun Lake, Isle Lake | Helisoma trivolvis | Unidentified | MH369473, MH369472, MH369476, MH369474, MH369475 | Present study | ||
| Renicolidae | Renicola sp. | Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | California Gull, Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | |
| Schistosomatidae | Austrobilharzia sp. | Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | |
| Avian Schistosomatid sp. A | Cercaria | Canada: Alberta, Buffalo Lake, Isle Lake | Physella gyrina | Unidentified | MH168789, MH168790, MH168795, MH168796 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | |
| Avian Schistosomatid sp. B | Cercaria | Canada: Alberta, Lac La Nonne | Physella gyrina | Unidentified | MH168785 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | |
| Avian Schistosomatid sp. C | Cercaria | Canada: Alberta, Wabamun Lake | Helisoma trivolvis | Unidentified | MH168793 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | |
| Schistosomatium douthitti | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KT831376 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake, Wabamun Lake | Stagnicola elodes, Lymnaea stagnalis | Unidentified | MH168791, MH168794 | Present study | ||
| Trichobilharzia cameroni | Cercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | ||
| Trichobilharzia physellae | Canada: Alberta, Lac La Nonne | Physella gyrina | Unidentified | MH168784 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | ||
| Cercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | |||
| Trichobilharzia stagnicolae | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH168781, MH168782, MH168786, MH168787, MH168788 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | |
| Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | KT831352 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Trichobilharzia szidati | Cercaria | Canada: Alberta, Gull Lake | Lymnaea stagnalis | Unidentified | MH168783 | Gordy, M.A., et al., 2018, Env. Health. 17(1):73 | |
| Cercaria | Canada: Alberta, Buffalo Lake | Lymnaea stagnalis | Unidentified | KT831375 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | ||
| Strigeidae | Apatemon gracilis | Cercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | |
| Adult | 13 Lakes in Alberta | Unidentified | Lesser Scaup | Bush, A.O. and Holmes, J.C., 1986, Can. J. Zool. 64:132‐141 | |||
| Larval | Cold Lake (54.30'N, 110W) | Unidentified | 9‐spine stickleback | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | |||
| Adult | 9 lakes in Alberta | Unidentified | Aechmophorus occidentalis, Podiceps grisegena, Podiceps nigricollis, Podiceps auritus | Stock, T.M. and Holmes, J.C., 1988, JP, 74(2): 214‐227 | |||
| Adult | Alberta | Unidentified | Chen hyperborea and Mareca americana | Palmieri, J.R., 1973, JP, 59(6):1063 | |||
| Apatemon sp. A | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH369603, MH369604, MH369605, MH369606, MH369607, MH369608, MH369609, MH369610, MH369611, MH369612, MH369613, MH369614, MH369615, MH369616, MH369617 | Present study | |
| Apatemon sp. B | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH369618 | Present study | |
| Apatemon sp. C | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH369619, MH369620, MH369621, MH369622 | Present study | |
| Apharyngostrigea pipientis | Adult | Eastern Alberta | Unidentified | Western Chorus Frog | Goldberg, S.R., Bursey, C.R., and Wong, C., 2002, Northwest Science, 76(1) | ||
| Australapatemon burti LIN1 | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | KT831346, KT831351 | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne, Gull Lake, Buffalo Lake | Stagnicola elodes, Physa gyrina, Helisoma trivolvis, Helisoma campanulatum, Planorbis sp., Lymnaea stagnalis | Unidentified | KY207548, KY207549, KY207551, KY207552, KY207553, KY207554, KY207555, KY207556, KY207559, KY207560, KY207561, KY207562, KY207563, KY207564, KY207565, KY207566, KY207567, KY207568, KY207570, KY207571, KY207572, KY207573, KY207574, KY207575, KY207576, KY207578, KY207579, KY207580, KY207581, KY207584, KY207585, KY207586, KY207588, KY207589, KY207590, KY207591, KY207592, KY207593, KY207594, KY207595, KY207598, KY207599, KY207600, KY207601, KY207602, KY207603, KY207604, KY207605, KY207606, KY207607, KY207608, KY207609, KY207610, KY207611, KY207612, KY207614, KY207617, KY207618, KY207619, KY207620, KY207621, KY207623, KY207624, KY587399, KY587398, KY587394, KY587401, HM385485, KY587400, HM385486 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | ||
| Cercaria | Canada: Alberta, Isle Lake, Wabamun Lake, Lac La Nonne, Gull Lake, Buffalo Lake | Stagnicola elodes, Physa gyrina, Helisoma trivolvis | Unidentified | MH369623, MH369624, MH369625, MH369626, MH369627, MH369628, MH369629, MH369630, MH369631, MH369632, MH369633, MH369634, MH369635, MH369636, MH369637, MH369638, MH369639, MH369640, MH369641, MH369642, MH369643, MH369644, MH369645, MH369646, MH369647, MH369648, MH369649, MH369650, MH369651, MH369652, MH369653, MH369654, MH369655, MH369656, MH369657, MH369658, MH369659, MH369660, MH369661, MH369662, MH369663, MH369664, MH369665, MH369666, MH369667, MH369668, MH369669, MH369670, MH369671, MH369672, MH369673, MH369674, MH369675, MH369676, MH369677, MH369678, MH369679, MH369680, MH369681, MH369682, MH369683, MH369684, MH369686, MH369687, MH369688, MH369689, MH369690, MH369691, MH369692, MH369693, MH369694, MH369695, MH369696, MH369697, MH369698, MH369699, MH369700, MH369701, MH369702, MH369703, MH369704, MH369705, MH369706, MH369707, MH369708, MH369709, MH369710, MH369711, MH369712, MH369713, MH369714, MH369715, MH369716, MH369717, MH369718, MH369719, MH369720, MH369721, MH369722, MH369723, MH369724, MH369725, MH369726, MH369727, MH369728, MH369729, MH369730, MH369731, MH369732, MH369733, MH369734, MH369735, MH369736, MH369737, MH369738, MH369739, MH369740, MH369741, MH369742, MH369743, MH369744, MH369745, MH369746, MH369747, MH369748, MH369749, MH369750, MH369751, MH369752, MH369753, MH369754, MH369755, MH369756, MH369757, MH369758, MH369759, MH369760, MH369761, MH369762, MH369763, MH369685 | Present study | ||
| Australapatemon mclaughlini | Cercaria, Adult | Canada: Alberta, Buffalo Lake; Ontario | Physa gyrina | Anas acuta | KY207615, KY207627, KY207628 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Buffalo Lake | Physa gyrina | MH369764 | Present study | |||
| Australapatemon sp. LIN2 | Adult | Canada: Ontario | Unidentified | Bucephala albeola | HM385535 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Australapatemon sp. LIN3 | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KY207577 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Australapatemon sp. LIN4 | Cercaria, Adult | Canada: Alberta, Lac La Nonne; Ontario | Physella gyrina | Aythya collaris | KY207569, KY587397, KY587396 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Gull Lake | Physa gyrina | Unidentified | MH369765 | Present study | ||
| Australapatemon sp. LIN5 | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | KY207597 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Australapatemon sp. LIN6 | Cercaria | Canada: Alberta, Pigeon Lake, Isle Lake | Physa gyrina | Unidentified | KY207613, KY207616 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Isle Lake, Buffalo Lake, Lac La Nonne | Physa gyrina | Unidentified | MH369766, MH369767, MH369768, MH369769, MH369770 | Present study | ||
| Australapatemon sp. LIN8 | Cercaria, Adult | Canada: Alberta, Isle Lake, Buffalo Lake; Ontario | Physa gyrina | Oxyura jamaicensis | KY207587, KY207622, HM385538, HM385537, HM385536 | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Isle Lake, Buffalo Lake, Gull Lake | Physa gyrina | Unidentified | MH369771, MH369772, MH369773, MH369774, MH369775, MH369776, MH369777 | Present study | ||
| Australapatemon sp. LIN9A | Cercaria, Adult | Canada: Alberta, Gull Lake, Isle Lake, Buffalo Lake; Ontario | Stagnicola elodes | Anas acuta | KY207550§, KY207557§, KY207558§, KY207582§, KY207596§, HM385534§ | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Lac La None, Gull Lake, Buffalo Lake, Isle Lake | Stagnicola elodes, Lymnaea stagnalis (MGC176B) | Unidentified | MH369779, MH369780, MH369781, MH369782, MH369783, MH369784, MH369785, MH369786, MH369787, MH369788, MH369789, MH369778 | Present study | ||
| Australapatemon sp. LIN9B | Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | KY207583§ | Gordy, M.A., et al., 2017, Parasitol. Res. 116(8): 2181‐98. | |
| Cercaria | Canada: Alberta, Buffalo Lake | Stagnicola elodes | Unidentified | MH369790, MH369791, MH369792 | Present study | ||
| Australapatemon sp. LIN10 | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | MH369793 | Present study | |
| Cercariae douglasi | Cercaria/Metacercaria | Lake Wabamun (114.35'W, 53.32'N) | Physa gyrina | Unidentified | Sankurathri, C.S. and Holmes, J.C., 1976, Can. J. Zool. 54:1742‐1753 | ||
| Cotylurus cornutus | Cercaria | Canada: Alberta, Gull Lake | Stagnicola elodes | Unidentified | KT831347§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Gull Lake, Isle Lake, Lac La Nonne | Stagnicola elodes, Helisoma trivolvis (MGC205) | Unidentified | MH369478, MH369480, MH369484, MH369485, MH369486, MH369487, MH369488, MH369489, MH369490, MH369491, MH369492, MH369493, MH369494, MH369495, MH369496, MH369497, MH369498, MH369500, MH369501, MH369502, MH369503, MH369504, MH369505, MH369509, MH369510, MH369511, MH369516, MH369532, MH369538, MH369539, MH369544, MH369557, MH369597, MH369601 | Present study | ||
| Cotylurus erraticus | Larval | Cold Lake (54.30'N, 110W) | Unidentified | White sucker, Whitefish, Cisco | Leong, T.S. and Holmes, J.C., 1981, J. Fish Biol. 18:693‐713 | ||
| Larval | Big Fish Lake, Caribou Lake, Eva Lake, Fleming Lake, Margaret Lake, Pitchimi Lake, Semo Lake, Sucker Lake, Wentzel Lake | Unidentified | Various fish species | Baldwin, R.E. and Goater, C.P., 2003, JP, 89(2):215‐225 | |||
| Adult | Beaverhill Lake (53.30'N, 112.30'W) and Miquelon Lake (53.15'N, 112.55'W) | Unidentified | Ring‐billed Gulls | Vermeer, K. 1969, Can. J. Zool. 47:267‐270 | |||
| Cotylurus flabelliformis | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | MH369519 | Present study | |
| Cotylurus hebraicus | Adult | 13 Lakes in Alberta | Unidentified | Lesser Scaup | Bush, A.O. and Holmes, J.C., 1986, Can. J. Zool. 64:132‐141 | ||
| Cotylurus marcogliesei | Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake, Isle Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369479, MH369481, MH369515, MH369530, MH369531, MH369553, MH369564 | Present study | |
| Cotylurus strigeoides | Cercaria | Canada: Alberta, Buffalo Lake, Wabamun Lake, Isle Lake, Lac La Nonne | Physa gyrina | Unidentified | MH369517, MH369518, MH369525, MH369526, MH369527, MH369528, MH369529, MH369560, MH369571, MH369572, MH369574, MH369575, MH369577, MH369583, MH369584, MH369587, MH369588, MH369590, MH369595, MH369596, MH369599, MH369600 | Present study | |
| Cotylurus sp. A | Cercaria | Canada: Alberta, Isle Lake | Stagnicola elodes | Unidentified | KT831371§ | Gordy, M.A., et al., 2016, Parasitol. Res. 115(10): 3867‐80. | |
| Cercaria | Canada: Alberta, Isle Lake, Lac La Nonne, Wabamun | Stagnicola elodes, Physa gyrina (MGC1962) | Unidentified | MH369513, MH369520, MH369521, MH369522, MH369523, MH369524, MH369533, MH369537, MH369541, MH369542, MH369543, MH369545, MH369546, MH369547, MH369548, MH369549, MH369550, MH369551, MH369552, MH369554, MH369555, MH369556, MH369558, MH369559, MH369561, MH369562, MH369573, MH369578, MH369579, MH369580, MH369581, MH369582, MH369585, MH369589, MH369591, MH369594, MH369598, MH369602 | Present study | ||
| Cotylurus sp. B | Cercaria | Canada: Alberta, Isle Lake | Physa gyrina | Unidentified | MH369586 | Present study | |
| Cotylurus sp. C | Cercaria | Canada: Alberta, Buffalo Lake | Lymnaea stagnalis | Unidentified | MH369563, MH369566, MH369576 | Present study | |
| Cotylurus sp. D | Cercaria | Canada: Alberta, Buffalo Lake | Physa gyrina | Unidentified | MH369592 | Present study | |
| Cotylurus sp. E | Cercaria | Canada: Alberta, Buffalo Lake, Gull Lake, Isle Lake, Lac La Nonne | Stagnicola elodes | Unidentified | MH369482, MH369483, MH369499, MH369506, MH369507, MH369508, MH369534, MH369535, MH369536, MH369540, MH369565, MH369593 | Present study | |
| Cotylurus sp. F | Cercaria | Canada: Alberta, Buffalo Lake, Wabamun Lake | Lymnaea stagnalis | Unidentified | MH369512, MH369514, MH369567, MH369568, MH369569, MH369570 | Present study | |
| Unknown | Choledocystus pennsylvaniensis | Adult | Eastern Alberta | Unidentified | Western Chorus Frog | Goldberg, S.R., Bursey, C.R., and Wong, C., 2002, Northwest Science, 76(1) |
Sequence updated in present study
Gordy MA, Hanington PC. A fine‐scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecol Evol. 2019;9:3153–3238. 10.1002/ece3.4939
DATA ACCESSIBILITY
DNA sequences: GenBank accessions MH368808–MH369793, KT831346–KT831348, KT831353, KT831356, KT831357, KT831359, KT831360, KT831363, KT831366, KT831371, KT831372, KT831377, KT831378, KT831382, KY207550, KY207557, KY207558, KY207582, KY207583, and KY207596. Sequence alignments and phylogenetic trees: TreeBASE (read only access until manuscript is approved) http://purl.org/phylo/treebase/phylows/study/TB2:S23234?x-access-code=c870e4e7ccd090a8c9a0ad25ac312dee&format=html. Host and location data: in Table 3.
REFERENCES
- Adlard, R. , & O'Donoghue, P. (1998). Perspectives on the biodiversity of parasitic protozoa in Australia. International Journal for Parasitology, 28(6), 887–897. [DOI] [PubMed] [Google Scholar]
- Adlard, R. D. , Miller, T. L. , & Smit, N. J. (2015). The butterfly effect: Parasite diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitology, 31, 160–166. 10.1016/J.PT.2014.11.001 [DOI] [PubMed] [Google Scholar]
- Altschul, S. F. , Gish, W. , Miller, W. , Myers, E. W. , & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. 10.1016/S0022-2836(05)80360-2 [DOI] [PubMed] [Google Scholar]
- Behrmann-Godel, J. (2013). Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): New insights through a combined morphological and genetic approach. Parasitol, 140(4), 509–520. [DOI] [PubMed] [Google Scholar]
- Bergmame, L. , Huffman, J. , Cole, R. , Dayanandan, S. , Tkach, V. V. , & McLaughlin, J. D. (2011). Sphaeridiotrema globulus and Sphaeridiotrema pseudoglobulus (Digenea): Species differentiation based on mtDNA (Barcode) and partial LSU–rDNA sequences. Journal of Parasitology, 97(6), 1132–1136. [DOI] [PubMed] [Google Scholar]
- Blankespoor, H. (1977). Notes on the biology of Plagiorchis noblei Park, 1936 (Trematoda: Plagiorchiidae). Proceedings of the Helminthological Society, 44(1), 44–50. [Google Scholar]
- Blasco-Costa, I. , & Locke, S. A. (2017). Life history, systematics and evolution of the diplostomoidea poirier, 1886: Progress, promises and challenges emerging from molecular studies. Advances in Parasitology, 98, 167–225. 10.1016/bs.apar.2017.05.001 [DOI] [PubMed] [Google Scholar]
- Blasco-Costa, I. , Poulin, R. , & Presswell, B. (2016). Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: Linking and characterising life cycle stages with morphology and molecules. Parasitology Research, 115, 271–289. 10.1007/s00436-015-4744-0 [DOI] [PubMed] [Google Scholar]
- Bray, R. A. , Cribb, T. H. , Littlewood, D. T. J. , & Waeschenbach, A. (2016). The molecular phylogeny of the digenean family Opecoelidae Ozaki, 1925 and the value of morphological characters, with the erection of a new subfamily. Folia Parasitol (Praha), 63, 1–11. 10.14411/fp.2016.013 [DOI] [PubMed] [Google Scholar]
- Chibwana, F. D. , Blasco-Costa, I. , Georgieva, S. , Hosea, K. M. , Nkwengulila, G. , Scholz, T. , & Kostadinova, A. (2013). A first insight into the barcodes for African diplostomids (Digenea: Diplostomidae): Brain parasites in Clarias gariepinus (Siluriformes: Clariidae). Infection, Genetics and Evolution, 17, 62–70. [DOI] [PubMed] [Google Scholar]
- Cribb, T. H. , Bray, R. A. , Littlewood, D. T. J. , Pichelin, S. P. , Herniou, E. A. , & Warren, A. (2001). The Digenea In Littlewood D. T. J. (Ed.), Interrelationships of the Platyhelminthes (pp. 168–185). London: Taylor & Francis. [Google Scholar]
- Detwiler, J. T. , Bos, D. H. , & Minchella, D. J. (2010). Revealing the secret lives of cryptic species: Examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution, 55, 611–620. 10.1016/j.ympev.2010.01.004 [DOI] [PubMed] [Google Scholar]
- Detwiler, J. T. , Zajac, A. M. , Minchella, D. J. , & Belden, L. K. (2012). Revealing cryptic parasite diversity in a definitive host: Echinostomes in muskrats. Journal of Parasitology, 98, 1148–1155. 10.1645/GE-3117.1 [DOI] [PubMed] [Google Scholar]
- García-Varela, M. , Sereno-Uribe, A. L. , Pinacho-Pinacho, C. D. , Hernández-Cruz, E. , & Pérezponce de León, G. (2016). An integrative taxonomic study reveals a new species of Tylodelphys Diesing, 1950 (Digenea: Diplostomidae) in Central and Northern Mexico. Journal of Helminthology, 90(6), 668–679. 10.1017/S0022149X15000917 [DOI] [PubMed] [Google Scholar]
- Georgieva, S. , Kostadinova, A. , & Skirnisson, K. (2012). The life-cycle of Petasiger islandicus Kostadinova & Skirnisson, 2007 (Digenea: Echinostomatidae) elucidated with the aid of molecular data. Systematic Parasitology, 82(3), 177–183. 10.1007/s11230-012-9354-y [DOI] [PubMed] [Google Scholar]
- Georgieva, S. , Selbach, C. , Faltýnková, A. , Soldánová, M. , Sures, B. , Skírnisson, K. , & Kostadinova, A. (2013a). New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors, 6, 64 10.1186/1756-3305-6-64 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georgieva, S. , Soldánová, M. , Pérez-del-Olmo, A. , Dangel, D. R. , Sitko, J. , Sures, B. , & Kostadinova, A. (2013b). Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology, 43, 57–72. 10.1016/j.ijpara.2012.10.019 [DOI] [PubMed] [Google Scholar]
- Georgieva, S , Faltýnková, A , Brown, R , Blasco-Costa, I , Soldánová, M , Sitko, J , & Kostadniova, A . Echinostoma “revolutum” (Digenea: Echinostomatidae) species complex revisited: Species delimitation based on novel molecular and morphological data gathered in Europe. Parasit Vectors 2014;7:520 10.1186/s13071-014-0520-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gibson, DI , Bray, RA , & Harris, EA . Host-Parasite Database of the Natural History Museum, London: 2005. [Google Scholar]
- Gordy, M. A. , Cobb, T. P. , & Hanington, P. C. (2018). Swimmer's itch in Canada: A look at the past and a survey of the present to plan for the future. Environmental Health, 17, 73 10.1186/s12940-018-0417-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gordy, M. A. , Kish, L. , Tarrabain, M. , & Hanington, P. C. (2016). A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta Canada. Parasitology Research, 115(10), 3867–3880. 10.1007/s00436-016-5152-9 [DOI] [PubMed] [Google Scholar]
- Gordy, MA , Locke, SA , Rawlings, TA , Lapierre, AR , & Hanington, PC . Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): A phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp. Parasitology Research 2017;116:2181–2198. 10.1007/s00436-017-5523-x [DOI] [PubMed] [Google Scholar]
- Graczyk, T. K. , & Shiff, C. J. (1993a). Excystment in vitro of Cotylurus cornutus (Trematoda: Strigeidae) Metacercariae. Journal of Parasitology, 79, 448 10.2307/3283586 [DOI] [PubMed] [Google Scholar]
- Graczyk, T. K. , & Shiff, C. J. (1993b). Experimental infection of domestic ducks and rodents by Notocotylus attenuatus (Trematoda: Notocotylidae). Journal of Wildlife Diseases, 29, 434–439. 10.7589/0090-3558-29.3.434 [DOI] [PubMed] [Google Scholar]
- Guindon, S , Dufayard, JF , Lefort, V , Anisimova, M , Hordijk, W , & Gascuel, O . New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 2010;59:307–321. 10.1093/sysbio/syq010 [DOI] [PubMed] [Google Scholar]
- Hernández-Cruz, E , Hernández-Orts, JS , Sereno-Uribe, AL , dePérez-Ponce León, G , & García-Varela, M . Multilocus phylogenetic analysis and morphological data reveal a new species composition of the genus Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae), parasites of fish-eating birds in the Americas. Journal of Helminthology 2018;92:572–595. 10.1017/s0022149x17000815 [DOI] [PubMed] [Google Scholar]
- Hernández-Mena, D. I. , García-Prieto, L. , & García-Varela, M. (2014). Morphological and molecular differentiation of parastrigea (Trematoda: Strigeidae) from Mexico, with the description of a new species. Parasitology International, 63(2), 315–323. 10.1016/j.parint.2013.11.012 [DOI] [PubMed] [Google Scholar]
- Hernández-Mena, DI , García-Varela, M , & dePérez-Ponce León, G . Filling the gaps in the classification of the Digenea Carus, 1863: Systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 2017; 94:833 10.1007/s11230-017-9745-1 [DOI] [PubMed] [Google Scholar]
- Herrmann, K. K. , Poulin, R. , Keeney, D. B. , & Blasco-Costa, I. (2014). Genetic structure in a progenetic trematode: Signs of cryptic species with contrasting reproductive strategies. International Journal for Parasitology, 44, 811–818. 10.1016/j.ijpara.2014.06.006 [DOI] [PubMed] [Google Scholar]
- Hoberg, EP , Galbreath, KE , Cook, JA , Kutz, SJ , & Polley, L . Northern Host-Parasite Assemblages . History and biogeography on the borderlands of episodic climate and environmental transition. vol. 79. Elsevier; 2012; 79:1–97. 10.1016/b978-0-12-398457-9.00001-9 [DOI] [PubMed] [Google Scholar]
- Huelsenbeck, J. P. , & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755. 10.1093/bioinformatics/17.8.754 [DOI] [PubMed] [Google Scholar]
- Jensen, K. , & Bullard, S. A. (2010). Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. International Journal for Parasitology, 40, 889–910. 10.1016/J.IJPARA.2009.11.015 [DOI] [PubMed] [Google Scholar]
- Kearse, M. , Moir, R. , Wilson, A. , Stones-Havas, S. , Cheung, M. , Sturrock, S. , … Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. 10.1093/bioinformatics/bts199 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keas, B. E. , & Blankespoor, H. D. (1997). The prevalence of Cercariae from Stagnicola emarginata (Lymnaeidae) over 50 years in Northern Michigan. Journal of Parasitology, 83, 536 10.2307/3284427 [DOI] [PubMed] [Google Scholar]
- Kostadinova, A. , & Herniou, E. (2003). Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology, 54(3), 159–176. [DOI] [PubMed] [Google Scholar]
- Kudlai, O. , Kostadinova, A. , Pulis, E. E. , & Tkach, V. V. (2015). A new species of Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae) from the double-crested cormorant Phalacrocorax auritus (Lesson) (Aves: Phalacrocoracidae) in North America. Systematic Parasitology, 90(3), 221–230. 10.1007/s11230-015-9550-7 [DOI] [PubMed] [Google Scholar]
- Kuhn, J. A. , Kristoffersen, R. , Knudsen, R. , Jakobsen, J. , Marcogliese, D. J. , Locke, S. A. , & Amundsen, P.-A. (2015). Parasite communities of two three-spined stickleback populations in subarctic norway—effects of a small spatial-scale host introduction. Parasitology Research, 114(4), 1327-1339. https://doi:10.1007/s00436-015-4309-2. [DOI] [PubMed] [Google Scholar]
- Kumar, S , Stecher, G , & Tamura, K . MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 2016;33:msw054 10.1093/molbev/msw054 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu, Z-X , Zhang, Y , Liu, Y‐T , Chang, Q‐C , Su, X , Fu, X , & Wang, C-R . Complete mitochondrial genome of Echinostoma hortense (Digenea: Echinostomatidae). Korean Journal of Parasitology 2016;54:173–179. 10.3347/kjp.2016.54.2.173 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Locke, SA , McLaughlin, JD , Dayanandan, S , & Marcogliese, D. J. Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 2010a;40:333–343. 10.1016/j.ijpara.2009.08.012 [DOI] [PubMed] [Google Scholar]
- Locke, S. A. , McLaughlin, J. D. , & Marcogliese, D. J. (2010b). DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater. Molecular Ecology, 19, 2813–2827. [DOI] [PubMed] [Google Scholar]
- Locke, S. A. , McLaughlin, J. D. , Lapierre, A. R. , Johnson, P. T. J. , & Marcogliese, D. J. (2011). Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. Journal of Parasitology, 97(5), 846–851. 10.1645/GE-2775.1 [DOI] [PubMed] [Google Scholar]
- Locke, S. A. , Al-Nasiri, F. S. , Caffara, M. , Drago, F. , Kalbe, M. , Lapierre, A. R. , McLaughlin, J. D. , … Marcogliese, D. J. (2015). Diversity, specificity and speciation in larval diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology, 45(13), 841–855. 10.1016/j.ijpara.2015.07.001 [DOI] [PubMed] [Google Scholar]
- Locke, S. A. , Van Dam, A. , Caffara, M. , Pinto, H. A. , López-Hernández, D. , & Blanar, C. A. (2018). Validity of the diplostomoidea and diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal for Parasitology, 48(13), 1043–1059. 10.1016/J.IJPARA.2018.07.001 [DOI] [PubMed] [Google Scholar]
- Mathison, B. A. , & Pritt, B. S. (2014). Laboratory identification of arthropod ectoparasites. Clinical Microbiology Reviews, 27, 48–67. 10.1128/CMR.00008-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miura, O. , Kuris, A. , & Torchin, M. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology, 35, 793–801. [DOI] [PubMed] [Google Scholar]
- Mollaret, I. , Jamieson, B. G. , Adlard, R. D. , Hugall, A. , Lecointre, G. , Chombard, C. , & Justine, J. L. (1997). Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Molecular and Biochemical Parasitology, 90, 433–438. [DOI] [PubMed] [Google Scholar]
- Morgan, J. A. T. , & Blair, D. (1998). Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. International Journal for Parasitology, 28, 493–502. 10.1016/S0020-7519(97)00204-X [DOI] [PubMed] [Google Scholar]
- Moszczynska, A , Locke, SA , McLaughlin, JD , Marcogliese, DJ , & Crease, TJ . Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 2009;9 Suppl s1:75–82. 10.1111/j.1755-0998.2009.02634.x [DOI] [PubMed] [Google Scholar]
- Nadler, S. , & DE León, G. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: Implications for parasitology. Parasitology, 138, 1688–1709. [DOI] [PubMed] [Google Scholar]
- Nagataki, M , Tantrawatpan, C , Agatsuma, T , Sugiura, T , Duenngai, K , Sithithaworn, P , … Saijuntha, W . Mitochondrial DNA sequences of 37 collar-spined echinostomes (Digenea: Echinostomatidae) in Thailand and Lao PDR reveals presence of two species: Echinostoma revolutum and E. miyagawai . Infect Genet Evol, 2015; 35: 56–62. [DOI] [PubMed] [Google Scholar]
- O'Hear, M. , Pote, L. , Yost, M. , Doffitt, C. , King, T. , & Panuska, C. (2014). Morphologic and molecular identifications of digenetic trematodes in double-crested cormorants (Phalacrocorax auritus) from the Mississippi Delta. USA. J Wildlife Dis, 50(1), 42–49. [DOI] [PubMed] [Google Scholar]
- Oksanen, J , Blanchet, F. G. , Friendly, M , Kindt, R , Legendre, P , McGlinn, D , & Wagner, H . Vegan: Community ecology package 2018.
- Otachi, E. O. , Locke, S. A. , Jirsa, F , Fellner-Frank, C , & Marcogliese, DJ . Morphometric and molecular analyses of Tylodelphys sp. Metacercariae (Digenea: Diplostomidae) from the vitreous humour of four fish species from lake Naivasha, Kenya. Journal of Helminthology 2015; 89(4): 404–414. 10.1017/s0022149x14000170 [DOI] [PubMed] [Google Scholar]
- Pérez-Ponce de León, G , & Poulin, R . An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology 2018;92:197–202. 10.1017/s0022149x17000189 [DOI] [PubMed] [Google Scholar]
- Pinto, H. A. , Griffin, M. J. , Quiniou, S. M. , Ware, C , & Melo, A. L. . Biomphalaria straminea (Mollusca: Planorbidae) as an intermediate host of Drepanocephalus spp. (Trematoda: Echinostomatidae) in Brazil: A morphological and molecular study. Parasitology Research 2016; 115(1): 51–62. 10.1007/s00436-015-4469-0 [DOI] [PubMed] [Google Scholar]
- Poulin, R. (2014). Parasite biodiversity revisited: Frontiers and constraints. International Journal for Parasitology, 44, 581–589. 10.1016/J.IJPARA.2014.02.003 [DOI] [PubMed] [Google Scholar]
- Poulin, R. , Besson, A. A. , Morin, M. B. , & Randhawa, H. S. (2016). Missing links: Testing the completeness of host-parasite checklists. Parasitology, 143, 114–122. 10.1017/S0031182015001559 [DOI] [PubMed] [Google Scholar]
- Poulin, R. , & Jorge, F. (2018). The geography of parasite discovery across taxa and over time. Parasitology, 1–8. 10.1017/S003118201800118X [DOI] [PubMed] [Google Scholar]
- Poulin, R , & Morand, S . Parasite Biodiversity. Smithsonian Books; 2004. 10.1645/ge-702r.1 [DOI] [Google Scholar]
- Puillandre, N. , Lambert, A. , Brouillet, S. , & Achaz, G. (2012). ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. 10.1111/j.1365-294X.2011.05239.x [DOI] [PubMed] [Google Scholar]
- R Core Team . R: A language and environment for statistical computing 2017.
- Roeber, F. , Jex, A. R. , & Gasser, R. B. (2013). Advances in the diagnosis of key gastrointestinal nematode infections of livestock, with an emphasis on small ruminants. Biotechnology Advances, 31, 1135–1152. 10.1016/J.BIOTECHADV.2013.01.008 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosser, T. G. , Baumgartner, W. A. , Alberson, N. R. , Woodyard, E. T. , Reichley, S. R. , Wise, D. J. , … Griffin, M. J. . Austrodiplostomum sp., Bolbophorus sp.(Digenea: Diplostomidae), and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae in inland silverside Menidia beryllina from catfish aquaculture ponds, with notes on the infectivity of Austrodiplostomum sp. cercariae in channel catfish Ictalurus punctatus. Parasitology Research 2016; 115(11): 4365–4378. [DOI] [PubMed] [Google Scholar]
- Schell, S. C. (1985). Handbook of the trematodes of North America north of Mexico. Moscow (Idaho): University Press Idaho. [Google Scholar]
- Schwelm, J. , Soldánová, M. , Vyhlídalová, T. , Sures, B. , & Selbach, C. (2018). Small but diverse: Larval trematode communities in the small freshwater planorbids Gyraulus albus and Segmentina nitida (Gastropoda: Pulmonata) from the Ruhr River, Germany. Parasitology Research, 117, 241–255. 10.1007/s00436-017-5699-0 [DOI] [PubMed] [Google Scholar]
- Selbach, C. , Soldánová, M. , Georgieva, S. , Kostadinova, A. , Kalbe, M. , & Sures, B. (2014). Morphological and molecular data for larval stages of four species of Petasiger Dietz, 1909 (Digenea: Echinostomatidae) with an updated key to the known cercariae from the palaearctic. Systematic Parasitology, 89(2), 153–166. 10.1007/s11230-014-9513-4 [DOI] [PubMed] [Google Scholar]
- Selbach, C , Soldánová, M , Georgieva, S , Kostadinova, A , & Sures, B . Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi'species complex.” Parasit Vectors 2015; 8(1): 300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snyder, S. D. , & Tkach, V. V. (2001). Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433 10.2307/3285315 [DOI] [PubMed] [Google Scholar]
- Soldánová, M. , Georgieva, S. , Roháčová, J. , Knudsen, R. , Kuhn, J. A. , Henriksen, E. H. , … Kostadinova, A. (2017). Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology, 47, 327–345. 10.1016/j.ijpara.2016.12.008 [DOI] [PubMed] [Google Scholar]
- Stoyanov, B. , Georgieva, S. , Pankov, P. , Kudlai, O. , Kostadinova, A. , & Georgiev, B. B. (2017). Morphology and molecules reveal the alien Posthodiplostomum centrarchi Hoffman, 1958 as the third species of Posthodiplostomum Dubois, 1936 (Digenea: Diplostomidae) in Europe. Systematic Parasitology, 94, 1–20. 10.1007/s11230-016-9680-6 [DOI] [PubMed] [Google Scholar]
- Tkach, V. V. , Kudlai, O. , & Kostadinova, A. (2016). Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology, 46, 171–185. 10.1016/J.IJPARA.2015.11.001 [DOI] [PubMed] [Google Scholar]
- Van Steenkiste, N. , Locke, S. A. , Castelin, M. , Marcogliese, D. J. , & Abbott, C. L. (2014). New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources, 15, 945–952. 10.1111/1755-0998.12358 [DOI] [PubMed] [Google Scholar]
- Vaughan, JA , Tkach, VV , & Greiman, SE . Neorickettsial endosymbionts of the digenea: Diversity, transmission and distribution. vol. 79. Elsevier; 2012. 10.1016/b978-0-12-398457-9.00003-2 [DOI] [PubMed] [Google Scholar]
- Vilas, R. , Criscione, C. , & Blouin, M. (2005). A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology, 131, 1–8. [DOI] [PubMed] [Google Scholar]
- Wickham, H , Francois, R , Henry, L , & Müller, K . dplyr: A grammar of data manipulation. R package 2017.
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
DNA sequences: GenBank accessions MH368808–MH369793, KT831346–KT831348, KT831353, KT831356, KT831357, KT831359, KT831360, KT831363, KT831366, KT831371, KT831372, KT831377, KT831378, KT831382, KY207550, KY207557, KY207558, KY207582, KY207583, and KY207596. Sequence alignments and phylogenetic trees: TreeBASE (read only access until manuscript is approved) http://purl.org/phylo/treebase/phylows/study/TB2:S23234?x-access-code=c870e4e7ccd090a8c9a0ad25ac312dee&format=html. Host and location data: in Table 3.