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. 2023 Jul 20;13(7):e10356. doi: 10.1002/ece3.10356

Short stories from Sphagnum of rare species, taxonomy, and speciation

Magni Olsen Kyrkjeeide 1,✉, Olena Meleshko 2, Kjell Ivar Flatberg 2, Kristian Hassel 2
PMCID: PMC10361360  PMID: 37484930

Abstract

Conserving species and their genetic variation are a global priority to safeguard evolutionary potential in a rapidly changing world. Species are fundamental units in research and nature management, but taxonomic work is increasingly undermined. Increasing knowledge on the species genetic diversity would aid in prioritizing conservation efforts. Sphagnum is a diverse, well‐known bryophyte genus, which makes the genus suited to study speciation and cryptic variation. The species share specific characteristics and can be difficult to separate in the field. By combining molecular data with thorough morphological examination, new species have recently been discovered. Still, there are taxonomic uncertainties, even for species assessed on the IUCN Red List of threatened species. Here, we use molecular data to examine three rare species within the subgenus Acutifolia described based on morphological characters. All species have narrow distributions and limited dispersability. First, we confirm the genetic origin of S. skyense. Second, we show that S. venustum is a haploid species genetically distinct from morphologically similar species. Lastly, S. nitidulum was found to have a distinct haplotype, but cannot be genetically separated from other red Acutifolia species. We also found high genetic variation within red Acutifolia specimens, indicating the need of further morphological examination and possibly taxonomic revision. Until then, our results have shown that genetic data can aid in prioritizing targets of conservation efforts when taxonomy is unresolved. All three taxa should be further searched for by field biologists to increase knowledge about their distribution ranges.

Keywords: genetic structure, microsatellites, molecular data, morphology, peatmosses, speciation, species identification

We used molecular data to resolve taxonomic uncertainty of three rare Sphagnum species described based on morhological characters. We confirm the parents of Sphagnum skyense and validate the species status of S. venustum. Sphagnum nitidulum has a distinct haplotype, but more data are needed to conclude whether it is a valid species.

graphic file with name ECE3-13-e10356-g005.jpg

1. INTRODUCTION

Recognizing and describing species is an essential task in biology, as species are the fundamental biodiversity units used in many research fields and nature management. Correct species identification is crucial to, for instance, obtain species distribution maps and biodiversity estimates, which are commonly used in a wide range of ecological studies (Stropp et al., 2022). Also, conservation efforts are usually targeting species, and global, regional, and national Red lists make assessments at the species level. Furthermore, the inclusion of genetic data in conservation management and prioritizations is becoming increasingly recognized, as maintaining genetic diversity can make species more resilient to rapid environmental changes (Andrello et al., 2022). In fact, maintaining genetic diversity within species to safeguard their adaptive potential is listed under Goal A in the “Kunming‐Montreal Biodiversity Framework” (CBD, 2022). Thus, increasing knowledge about diversity among and within species is highly important to make informed decisions about where conservation efforts should be applied.

The genus Sphagnum L. is species‐rich and one of the most studied bryophyte genera, partly because it is the main driver of peat accumulation in boreal peatlands. Consequently, Sphagnum stores more carbon than any other plant genera (Yu et al., 2011). Evolutionary, the genus is on a long branch separated from the rest of the mosses, but with relatively recent, rapid diversification (Shaw et al., 2010). A major driver of speciation in Sphagnum seems to be adaptation to niches along the water table gradient within the mire landscape (Johnson et al., 2015; Rydin, 1986). Another important speciation mechanism is allopolyploidization, a process where two species hybridize and give viable offspring. Around 20% of Sphagnum species have originated as a result of allopolyploidization (Meleshko et al., 2018). Allopatric speciation due to barriers like the Atlantic Ocean is much less prevalent in bryophytes than seed plants, as Europe and North America share the majority of moss species (Carter et al., 2016; Frahm & Vitt, 1993). This is mainly explained by effective dispersal of bryophyte spores (Heinrichs et al., 2009; Kyrkjeeide, Hassel, Flatberg, Shaw, Brochmann, & Stenoien, 2016; Szövenyi et al., 2008). High species diversity of Sphagnum is found in the boreal region, a paradox considering the short time since the last glacial maximum. High dispersibility leading to colonization may explain this, but the role of geographical isolation in driving speciation in bryophytes is not well‐understood (but see Yousefi et al., 2019).

Sphagnum species are morphologically similar and often display phenotypic plasticity (Stenøien et al., 2014), and closely related species may have overlapping niches (Hassel et al., 2018; Yousefi et al., 2017). Thus, species delineation has been a debated topic within Sphagnum biology (Cronberg, 1989; Flatberg, 1986). Lately, investigating genetic variation has aided the identification of new species, even within common and well‐studied species such as S. magellanicum Brid. sensu lato (Hassel et al., 2018; Kyrkjeeide, Hassel, Flatberg, Shaw, Yousefi, & Stenoien, 2016; Shaw et al., 2022; Yousefi et al., 2019). Despite the effort to describe Sphagnum diversity, there are still unresolved taxonomical issues, even for species assessed in the IUCN Red List of threatened species (Gabriel & Sim‐Sim, 2019).

Taxonomic work is time‐consuming, and becoming a species expert may take years of training in the field and/or identification of microscopical characters in the laboratory. Field trips enable experts to collect specimens and enroll them in scientific collections. These collections have value for scientific discoveries and as a historical record of biodiversity (Pyke & Ehrlich, 2010; Suarez & Tsutsui, 2004), but not if specimens stay hidden in storage. For example, S. beothuk Andrus, described from Newfoundland, Canada (Andrus, 2006), was not detected in Europe before it was discovered to be genetically the same as specimens collected for years as a “dark morph” of S. fuscum (Schimp.) H. Klinggr. (Kyrkjeeide et al., 2015). Also, within the widespread S. warnstorfii Russow, extensively used in ecological studies (Bengtsson et al., 2016; Granath et al., 2010; Hájek et al., 2021), European specimens belonging to different genotypes seem to hold morphological variation (Mikulášková et al., 2015).

Here, we use molecular data to explore genetic differentiation and to clarify the taxonomic status of three rare species from Sphagnum subgenus Acutifolia (Wilson) A.J. Shaw: S. skyense Flatberg, S. venustum Flatberg, and S. nitidulum Warnstorf. All three species are described solely based on morphological data (Figure 1).

FIGURE 1.

FIGURE 1

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Sphagnum skyense (left), S. venustum (middle), and S. nitidulum (right) are three rare species described based on morphological data. Photos: K.I. Flatberg.

Sphagnum skyense was detected as a distinct red‐colored peat moss in the heathland on Isle of Skye, Scotland, and later described as a new species based on morphology (Flatberg, 1988a). The large size of S. skyense and its morphological resemblance to both S. quinquefarium (Lindb.) Warnst. and S. subnitens Russow & Warnst. lead to the hypothesis that this likely was an allopolyploid species. Genetic analysis including most species in subgenus Acutifolia (except S. quinquefarium) confirmed the allopolyploid origin, but suggested S. warnstorfii and S. subnitens as the likely progenitors of S. skyense (Shaw et al., 2005). No further attempt has been made in studying the ploidy level or the origin of S. skyense, with the latter remaining an open question for more than 30 years.

Sphagnum venustum is one of the most recent contributions of new species in Acutifolia. It was discovered and described based on collections from Labrador, eastern Canada (Flatberg, 2008), and later several new localities were reported from Quebec, Canada (Ayotte & Rochefort, 2019). In 2011, it was also discovered in Norway, but so far from one single site. Hill (2019) asked whether this single site occurrence of S. venustum could be a result of separate hybridization events on different continents. However, we hypothesis that it is a haploid species due to the small size, as allopolyploids tend to be larger than their progenitors (Flatberg, 1988a, 1988b).

Sphagnum nitidulum was described in 1911 and is still only known from one site on the Azorean island Terceira. It grows on soil in warm spots in the sulfurous fumaroles—a very rare substrate for Sphagnum species (Séneca & Söderström., 2009). The species has been seen as conspecific with S. rubellum (Andrews, 1941), but anyhow been included on several checklists (Gabriel & Sim‐Sim, 2019 and references therein). The type was assumed to be destructed, but it was photographed in 1991 (Gabriel & Sim‐Sim, 2019). Collections from the type locality in herbarium TRH were obtained in 2004 (four specimens) and 2021 (two specimens). Sphagnum nitidulum is one of the “red Acutifolia species.” Within this group, species delineation of S. capillifolium and S. rubellum has been debated and thoroughly studied, concluding that the two species may overlap morphologically (Cronberg, 1989), but are genetically distinct (Cronberg, 1996, 1998). Morphological overlap has also been observed between specimens identified as both S. capillifolium and S. warnstorfii (K. I. Flatberg, personal communication). Such specimens have been collected in mainland Europe the last two decades and tagged under different provisional names (specimens in TRH). We included these specimens (hereafter called conspecific specimens) to explore whether S. nitidulum is genetically distinct from other red Acutifolia species and whether the observed morphological similarities between S. nitidulum and deviating specimens of S. warnstorfii and S. capillifolium are reflected in molecular data.

We aim to identify the parental species of S. skyense, confirm the haploid level and the genetic distinctness of S. venustum, and evaluate whether S. nitidulum is genetically distinct from other “red Acutifolia specimens.”

2. MATERIALS AND METHODS

We used 72 Sphagnum specimens from the scientific collection (herbarium TRH) in Trondheim, Norway, collected in Europe and Eastern Canada. An overview of species and number of specimens are given in Table 1. DNA was extracted from the apical part of gametophytes, that is the middle part of the capitula, for each specimen using the NucleoSpin Plant II, Mini kit for plant DNA (Macherey‐Nagel) or E.Z.N.A.® HP Plant DNA Mini Kit (Omega Bio‐tek), following the manufacturers' protocols. The ploidy level of bryophytes is based on the gametophytic phase. Most Sphagnum species are haploid, whereas allopolyploid species have diploid or triploid gametophytes.

TABLE 1.

Voucher information for Sphagnum specimens used in the molecular analyses.

DNA ID TRH ID Herb. assigned taxon Country Province/county Longitude Latitude Year Collector Assigned taxon in analyses
ss1 728,102 S. skyense Scotland Highland 1987 KIF Skyense
ss3 728,099 S. skyense Scotland Highland 2004 MOH Skyense
ss4 741,748 S. cf. skyense Ireland Tipperary 2005 NGH Skyense
ss5 93,374 S. subnitens ssp. subnitens Norway Vestland 4,97883 60,59546 2017 MJ, CP, MOK, KIF Subnitens
ss6 93,414 S. subnitens ssp. subnitens Norway Vestland 5,10753 59,99331 2017 MJ, CP, MOK, KIF Subnitens
ss7 728,280 S. subnitens ssp. subnitens Scotland Highland 1987 KIF Subnitens
ss8 120,164 S. subnitens ssp. subnitens Ireland Mayo −9,51535 54,10317 2011 MOK, KOK Subnitens
ss9 728,298 S. subnitens ssp. subnitens Wales Gwynedd 1980 KIF Subnitens
ss10 93,420 S. quinquefarium Norway Vestland 5,20637 59,59257 2017 MJ, CP, MOK, KIF Quinquefarium
ss11 93,405 S. quinquefarium Norway Vestland 5,10615 59,99316 2017 MJ, CP, MOK, KIF Quinquefarium
ss12 120,123 S. quinquefarium Scotland Highland −6,06299 57,17806 2011 MOK Quinquefarium
ss13 4802 S. quinquefarium Scotland Scottish Borders −2,85016 55,19173 2014 KH Quinquefarium
ss68 109,503 S. quinquefarium Scotland Highland −6,24462 57,42046 2019 NGH Quinquefarium
ss23 93,432 S. capillifolium Norway Vestland 5,19754 59,61486 2017 MJ, CP, MOK, KIF Capillifolium
ss24 673,473 S. capillifolium Scotland Highland 1987 KIF Capillifolium
ss26 13,176 S. capillifolium Scotland Highland −5,01957 58,19938 2015 KH Capillifolium
ss28 94,003 S. capillifolium Austria Salzburg 13,78167 47,08359 2017 KIF, CS Capillifolium
ss29 38,148 S. capillifolium Slovakia Prešov Region 20,22992 49,2195 2016 KH Capillifolium
ss30 98,303 S. capillifolium Slovakia Prešov Region 20,22212 49,21094 2016 KIF Capillifolium
ss31 93,386 S. capillifolium Norway Vestland 5,01412 60,56181 2017 MJ, CP, MOK, KIF Capillifolium
ss36 93,415 S. capillifolium Norway Vestland 5,10753 59,99331 2017 MJ, CP, MOK, KIF Capillifolium
ss37 93,414 S. capillifolium Norway Vestland 5,10753 59,99331 2017 MJ, CP, MOK, KIF Capillifolium
ss39 740,734 S. capillifolium Norway Trøndelag 10,41161 63,20311 2003 KIF Capillifolium
224 108,510 S. rubellum Norway Trøndelag 11,21917 64,23135 2019 KH, OM, MOK, KIF Conspecific
230 115,591 S. cf. capillifolium × warnstorfii Norway Trøndelag 9,099786 63,06362 2016 KIF Conspecific
241 148,557 S. cf. capillifolium × warnstorfii Norway Trøndelag 10,46162 63,38908 2019 KIF Conspecific
ss21 93,450 S. cf. warnstorfii Norway Vestland 5,19795 59,61641 2017 MJ, CP, MOK, KIF Conspecific
ss27 94,018 S. capillifolium Austria Salzburg 13,67968 47,08395 2017 KIF, CS Conspecific
ss34 94,041 S. cf. capillifolium × warnstorfii Austria Oberosterreich 12,95769 48,0541 2017 KIF Conspecific
ss35 94,020 S. cf. capillifolium × warnstorfii Austria Salzburg 13,67906 47,08405 2017 KIF, CS Conspecific
SW01 148,553 S. cf. warnstorfii Denmark Jylland 9,135816 56,37582 2021 IG Conspecific
SN11 727,588 S. cf. nitidulum Portugal Azores 2004 KIF Nitidulum
SN12* 121,476 S. nitidulum Portugal Azores −27,2 38,73333 2021 EFC Nitidulum
SN13* 121,475 S. nitidulum Portugal Azores −27,2167 38,73333 2021 EFC Nitidulum
SN14* 727,587 S. cf. nitidulum Portugal Azores 2004 KIF Nitidulum
RB01** 728,039 S. cf. rubellum Portugal Azores 2004 KIF Nitidulum
221 725,290 S. rubellum Canada Quebec −57,1541 51,43078 2007 BF, KIF Rubellum
222 725,305 S. rubellum Canada Newfoundland and Labrador −56,7302 51,57122 2007 BF, KIF Rubellum
223 37,834 S. rubellum Norway Trøndelag 11,43851 64,70585 2016 KH Rubellum
240 148,556 S. rubellum Norway Trøndelag 10,46162 63,38908 2019 KIF Rubellum
242 148,558 S. rubellum Norway Trøndelag 10,46162 63,38908 2019 KIF Rubellum
ss15 11,185 S. cf. warnstorfii Norway Vestland 5,16446 59,65667 2015 KH Rubellum
ss25 120,124 S. rubellum Scotland Highland −6,37338 57,37548 2011 MOK Rubellum
ss32 98,281 S. cf. capillifolium Czech Republic Pardubický kraj 15,96429 49,73827 2016 KIF Rubellum
ss33* 98,279 S. cf. capillifolium Czech Republic Pardubický kraj 15,96429 49,73827 2016 KIF Rubellum
ss61 158,861 S. rubellum Norway Trøndelag 10,06233 63,97804 2002 KIF Rubellum
ss63 725,288 S. rubellum Canada British Columbia −126 49,16667 2000 KIF Rubellum
229 115,591 S. warnstorfii Norway Trøndelag 9,099786 63,06362 2016 KIF Warnstorfii
ss14 728,537 S. warnstorfii Scotland Highland 1987 KIF Warnstorfii
ss16 740,618 S. warnstorfii Norway Vestland 5,64284 60,41393 2008 KIF Warnstorfii
ss17 38,119 S. warnstorfii Czech Republic Pardubický kraj 15,96413 49,73867 2016 KH Warnstorfii
ss18 98,276 S. warnstorfii Czech Republic Pardubický kraj 15,93139 49,70528 2016 KIF Warnstorfii
ss19 93,992 S. warnstorfii Austria Salzburg 13,86189 47,18654 2017 KIF, CS Warnstorfii
ss20 94,022 S. warnstorfii Austria Salzburg 13,7101 47,10077 2017 KIF, CS Warnstorfii
ss65 109,505 S. warnstorfii Scotland Highland −6,22782 57,4338 2019 NGH Warnstorfii
ss66 109,504 S. warnstorfii Scotland Highland −6,22782 57,4338 2019 NGH Warnstorfii
ss67 109,506 S. warnstorfii Scotland Highland −6,22782 57,4338 2019 NGH Warnstorfii
ss64 728,492 S. venustum Canada Newfoundland and Labrador −56,3042 51,97892 2007 BF, KIF Venustum
ss70 741,059 S. venustum Norway Trøndelag 11,69203 63,93091 2011 KIF Venustum
ss71 728,496 S. venustum Canada Quebec −72,6333 53,85 2010 MW Venustum
220 741,060 S. venustum Norway Trøndelag 11,69203 63,93091 2011 KIF Venustum
217 724,524 S. beothuk Canada Newfoundland and Labrador −56,7053 51,62902 2007 BF, KIF Beothuk
213 108,518 S. beothuk Norway Trøndelag 11,24113 64,57635 2019 KH, OM, MOK, KIF Beothuk
214 108,530 S. beothuk Norway Trøndelag 11,07712 64,4292 2019 KH, OM, MOK, KIF Beothuk
215 724,518 S. beothuk Canada Newfoundland and Labrador −55,6243 52,37197 2007 BF, KIF Beothuk
219 115,819 S. fuscum Canada Quebec −72,2329 52,81405 2018 LB, MFI Fuscum
210 724,520 S. fuscum Canada Quebec −57,2362 51,50422 2007 BF, KIF Fuscum
212 724,523 S. fuscum Canada Newfoundland and Labrador −56,7088 51,66303 2007 BF, KIF Fuscum
209 114,017 S. fuscum Norway Trøndelag 11,21456 64,26283 2020 KH, KIF, OM Fuscum
211 676,317 S. fuscum Norway Trøndelag 11,6934 63,93074 2013 TP Fuscum
ss58 158,973 S. fuscum Norway Trøndelag 10,51795 64,09067 2002 KIF Fuscum
ss60 724,509 S. fuscum Canada British Columbia 2000 KIF Fuscum
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Note: The specimens were analyzed in three different datasets: the Actuifolia dataset included all specimens except S. skyense and samples marked with * (assumed to be clones sampled at the same site), the ‘red Acutifolia’ dataset further excluded samples marked as ** (identical haplotypes), and the S. skyense dataset that included all individuals in bold. The specimen order in the table is the same as the specimen order in the boxplots in Figures 2 and 3 from left to right. Collectors: BF, B. Flatberg; CP, C. Pötsch; CS, C. Schröck; EF, E. Feldmayer‐Christe; IG, I. Goldberg; KH, K. Hassel; KIF, K.I. Flatberg; KOK, K.O. Kyrkjeeide; LB, L. Bourgouin; MFI, M.‐F. Indorf; MJ, M. Jokerud; MOH, M.O. Hill; MOK, M.O. Kyrkjeeide; MW, M. White; NGH, N.G. Hodgetts; OM, O. Meleshko; TP, T. Prestø.

We used microsatellite markers to explore genetic diversity of the specimens. These markers have been frequently used as a mean of identifying new species (e.g., Karlin et al., 2008) and genetic structuring patterns (Kyrkjeeide, Hassel, Flatberg, Shaw, Yousefi, & Stenoien, 2016), and they allow identification of ploidy levels as allopolyploid species have more than one allele present at several loci (Kyrkjeeide et al., 2019; Ricca et al., 2008). Furthermore, patterns obtained by microsatellite data has been confirmed using much larger SNP datasets (Duffy et al., 2020; Shaw et al., 2022). Altogether, 15 microsatellite markers (1, 7, 9, 12, 17, 19, 20, 22, 29, 30, 56, 65, 68, 78, 93) were amplified for all specimens and genotyped in GeneMapper (Table 2, see e.g., Kyrkjeeide, Hassel, Flatberg, Shaw, Brochmann, & Stenoien, 2016 for methods).

TABLE 2.

Allele data of Acutifolia specimens from 15 microsatellite markers (ssr) developed for Sphagnum.

DNA ID Assigned name in analyses ssr1 ssr7 ssr12 ssr68 ssr19 ssr93 ssr29 ssr30 ssr9 ssr56 ssr20 ssr22 ssr17 ssr65 ssr78
ss1 skyense 245 189/198 117 218/225 264 221/253 198 127/139 187/189 200/206 277/282 94/103 158/0 190 201/213
ss3 skyense 245 189/198 117 218/225 264 221/253 198 127/139 187/189 200/206 277/282 94/103 158/164 190 201/213
ss4 skyense 245 189/200 117 218/225 264 221/250 198 127/139 187/187 200/206 277/282 94/103 158/164 190 201/207
ss5 subnitens 245 189 117 225 264 221 198 127 187 209 282 94 164 190 207
ss6 subnitens 245 189 117 225 264 221 198 127 187 203 282 94 164 190 207
ss7 subnitens 245 189 117 225 264 221 198 127 187 203 282 94 164 190 207
ss8 subnitens 245 197 117 225 264 221 198 127 187 197 282 94 164 190 213
ss9 subnitens 245 189 117 225 264 221 198 127 187 197 282 94 164 190 207
ss10 quinquefarium 245 198 117 218 256 0 201 139 186 206 277 103 158 190 201
ss11 quinquefarium 245 198 117 218 256 250 198 139 189 206 277 103 156 190 201
ss12 quinquefarium 245 198 117 218 256 253 201 139 189 206 277 103 156 190 201
ss13 quinquefarium 245 198 117 218 256 0 198 139 186 206 277 103 158 190 201
ss68 quinquefarium 245 198 117 218 256 253 198 139 186 206 277 103 156 190 201
ss23 capillifolium 245 177 119 222 256 229 201 137 172 239 276 106 155 187 195
ss24 capillifolium 245 179 119 222 256 229 201 137 185 239 276 106 161 187 213
ss26 capillifolium 245 177 119 222 270 229 201 137 185 230 276 106 161 187 195
ss28 capillifolium 245 177 119 222 256 229 202 137 185 221 277 106 161 190 195
ss29 capillifolium 245 177 119 222 256 229 201 137 172 233 276 106 155 187 213
ss30 capillifolium 245 177 119 222 256 229 200 137 168 233 277 106 155 187 195
ss31 capillifolium 245 177 119 222 256 229 201 137 185 221 276 106 161 187 195
ss36 capillifolium 245 177 119 222 256 229 200 137 169 230 276 106 161 187 195
ss37** capillifolium 245 177 119 222 256 229 200 137 169 230 276 106 161 187 195
ss39 capillifolium 245 177 119 222 256 229 201 137 172 239 277 106 155 187 195
224 conspecific 245 177 119 225 258 229 198 137 185 215 274 109 155 184 210
230 conspecific 245 179 119 225 267 247 204 137 0 215 274 109 155 185 195
241 conspecific 245 186 123 223 256 229 198 137 184 215 274 112 157 190 210
ss21 conspecific 245 177 123 225 256 229 195 143 169 215 274 109 157 190 195
ss27** conspecific 245 0 119 223 264 229 198 137 162 224 274 112 157 184 195
ss34 conspecific 245 179 123 225 0 229 195 137 184 215 274 109 155 190 207
ss35 conspecific 245 0 119 223 264 229 198 137 162 224 274 112 157 184 195
SW01 conspecific 245 179 119 225 267 229 195 137 184 215 300 109 152 184 207
SN1*3* nitidulum 245 175 119 231 259 247 204 147 169 233 275 109 157 190 201
SN11 nitidulum 245 175 119 231 259 247 204 147 169 233 275 109 157 190 201
SN12* nitidulum 245 175 119 231 259 247 204 147 169 233 275 109 157 190 201
SN14* nitidulum 245 175 119 231 259 247 204 147 169 233 275 109 157 190 201
RB01** nitidulum 245 175 119 231 259 247 204 147 169 233 275 109 157 190 201
221 rubellum 245 177 119 231 264 232 198 137 195 221 277 112 155 0 216
222 rubellum 245 173 119 225 259 247 198 137 180 227 295 109 155 184 210
223 rubellum 245 0 119 225 264 241 195 137 0 230 295 112 157 196 207
240 rubellum 245 187 125 225 264 229 196 137 169 191 274 94 157 194 201
242 rubellum 245 179 125 225 263 241 200 147 179 224 298 109 157 190 210
ss15 rubellum 245 177 123 225 259 229 204 139 169 233 295 109 152 184 210
ss25 rubellum 245 179 119 225 266 244 201 143 169 224 274 106 152 184 204
ss32 rubellum 245 179 123 228 264 244 196 137 169 224 295 109 157 190 195
ss33* rubellum 245 179 123 228 264 244 196 137 169 224 295 109 157 190 195
ss61 rubellum 245 173 125 225 264 232 204 137 169 224 298 90 157 196 195
ss63 rubellum 245 181 123 225 274 232 196 147 172 218 274 106 152 194 201
229 warnstorfii 245 190 119 225 267 244 201 139 172 194 290 100 155 187 204
ss14 warnstorfii 245 194 119 225 270 244 201 141 172 188 289 100 155 181 204
ss16 warnstorfii 245 190 0 225 267 247 201 139 172 212 289 100 157 187 0
ss17 warnstorfii 245 190 121 225 267 247 201 141 172 224 289 100 155 187 195
ss18 warnstorfii 245 190 0 225 270 244 201 139 172 212 289 100 155 187 204
ss19 warnstorfii 245 190 117 225 267 243 201 139 179 212 292 103 155 187 204
ss20 warnstorfii 245 190 0 225 270 243 201 139 179 194 289 103 155 187 0
ss65** warnstorfii 245 190 119 0 269 244 201 141 196 221 289 103 155 181 0
ss66 warnstorfii 245 190 119 225 265 247 200 141 178 224 289 100 155 187 0
ss67 warnstorfii 245 190 119 225 269 244 201 141 196 221 289 103 155 181 201
220 venustum 245 175 119 218 282 251 198 137 196 227 277 106 155 191 204
ss64 venustum 245 175 119 218 279 251 201 147 196 227 277 106 155 191 195
ss70** venustum 245 175 119 218 282 251 0 137 196 227 277 106 155 191 204
ss71 venustum 245 175 119 218 273 251 195 143 196 227 277 106 155 191 204
217 beothuk 245 179 121 218 256 250 198 127 182 206 277 106 0 194 201
213 beothuk 245 179 121 218 256 238 198 127 182 206 277 106 157 194 201
214 beothuk 245 179 121 218 256 238 198 127 182 206 277 106 157 194 201
215 beothuk 245 179 121 218 0 247 198 127 182 206 277 106 157 194 201
219 fuscum 245 189 121 225 256 241 198 127 182 209 294 103 158 175 198
210 fuscum 245 189 121 225 256 241 198 130 186 212 288 103 158 176 198
212 fuscum 245 189 121 225 256 241 198 127 182 209 288 109 158 176 198
209 fuscum 245 193 121 225 256 241 198 130 182 212 288 97 158 176 198
211 fuscum 245 193 121 227 256 241 198 130 186 212 291 103 158 176 198
ss58 fuscum 245 189 121 225 256 241 198 130 186 215 291 106 158 176 198
ss60 fuscum 245 189 121 225 255 241 198 127 186 212 291 103 153 176 198
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Note: The DNA ID correspond to the ID in Table 1 and Figure 4. Specimens were analyzed in three different datasets (see main text and Table 1). The specimen order in the table is the same as the specimen order in the boxplots in Figures 2 and 3 from left to right. Sphagnum skyense named skyense under Assigned name in analyses, is diploid and have two alleles at each microsatellite.

After visually studying the number of alleles identified for each morphological species, three datasets were prepared for statistical analyses. The first dataset included all specimens identified as haploid (one allele at each locus), this only excluded S. skyense. In addition, four samples were excluded as they were collected at the same site and had identical haplotypes, and hence were likely clones (see Table 2). A total of 65 specimens were included in the dataset and we hereafter call it the Acutifolia dataset. The second dataset, hereafter called the “red Acutifolia” dataset, included specimens of S. rubellum, S. capillifolium, S. warnstorfii, S. nitidulum and conspecific specimens, and also S. venustum, as analyses of the Acutifolia dataset show that this species cluster with “red Acutifolia” (see below). Specimens with identical haplotypes were removed from the dataset, and a total of 39 specimens were analyzed. The third dataset, hereafter called the S. skyense dataset, included S. skyense and the hypothesized parental species: S. subnitens, S. quinqefarium, and S. warnstorfii. In total, 17 specimens were included in this dataset and scored as diploid individuals, with the second allele scored as missing for the three latter species.

The software Structure (Falush et al., 2003, 2007; Pritchard et al., 2000) was used to identify the number of genetic clusters and potential admixture among individuals of morphologically described taxa (sensu van Hengstum et al., 2012). The analysis was run for the first dataset with the number of genetic clusters (K) ranging from 1 to 10, to explore clustering among all Acutifolia species. The second dataset was run using K = 2–6. The dataset included five morphologically described species and seven specimens that were collected as conspecific (Table 1). The third dataset was run for K = 3, as S. skyense is described as a hybrid species and the aim of the analyses were to detect potential admixture between the parental species. For each K, the analyses were replicated 10 times with a burnin of 100,000 steps followed by a Monte Carlo Markov chain of 200,000 steps. We ran Structure with different settings for the first dataset applying the admixture model and both the correlated and independent allele frequencies model. The correlated allele frequencies model is better at detecting distinct populations that are closely related (Porras‐Hurtado et al., 2013), and this model was used when analyzing the second and third datasets. The results were further assessed using Clumpak (Kopelman et al., 2015) and visualized with StructureSelector (Li & Liu, 2017).

The data were also explored in GenAlEx v6.501 (Peakall & Smouse, 2012). A genetic distance matrix was made of the Acutifolia dataset and the “red Acutifolia” dataset using the haploid (ssr) option and interpolating missing data. The distance matrices were used in PCoA analyses with the covariance‐standardized method in GenAlEx, but for the Acutifolia dataset also in SplitsTree v4.19.0 (Huson & Bryant, 2006) to make a Neighbor‐Net network (Bryant & Moulton, 2002). A PCoA was also made for the S. skyense dataset, but the distance matrix was made with the codominant option and the haploid specimens scored as homozygotes to avoid missing data at the second allele.

3. RESULTS

We used the number of alleles recognized for each locus to confirm the ploidy level of S. skyense and S. venustum (sensu Ricca et al., 2008). Our results confirm that S. venustum is a haploid species, as only one allele was identified for each locus, while S. skyense is diploid as 10 of 15 loci have two alleles. At the five loci with only one allele, four of them have the same allele in S. skyense, S. subnitens and S. quinquefarium (Table 2). Furthermore, a visual comparison of alleles across the S. skyense dataset, shows that the alleles in the heterozygote loci are mainly the same as alleles found in S. subnitens and S. quinquefarium. The Structure analysis of this dataset shows that S. skyense is indeed admixed between S. subnitens and S. quinquefarium, strongly supporting that they are the parental species of S. skyense (Figure 2).

FIGURE 2.

FIGURE 2

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Microsatellite data of Sphagnum × skyense show that the species has two alleles at most of its loci, strongly indicating that it is a diploid species originating from hybridization. The barplot shows the result of STRUCTURE analysis of microsatellite data of S. × skyense and three hypothesized parental species. The result confirms that S. × skyense is an admixed species between S. subnitens and S. quinquefarium. This is also evident in the PCoA (below) which shows that S. × skyense is placed between its parental species. In the barplot, each bar represents one individual. The order of the bars, from left to right, follows the order of individuals listed in Table 1 (dataset S. × skyense).

Also, specimens of S. venustum had one allele at each loci, thus, the species is haploid. A sample collected as S. cf. rubellum in the Azores (Terceira) was genetically identical to the samples collected as S. nitidulum (Table 2). The Azores specimens share alleles with other Acutifolia species, but the same alleles overlap at maximum four loci with other specimens (Table 2). All the conspecific specimens had one allele at each locus; hence, they were all haploids, even though many of them were morphologically assigned as hybrids (Table 1).

The Structure analysis of the Acutifolia dataset shows that S. venustum mainly clusters with “red Acutifolia” species and that morphological species separate into different genetic clusters as the value of K increases. The Azorean specimens cluster with S. rubellum at K = 2–5, but as a separate cluster at K = 7–10. However, in analyses of the “red Acutifolia” dataset, where only unique haplotypes were included, the Azorean specimen cluster with S. rubellum at all K‐values (Figure 3). Furthermore, this analysis separates S. capillifolium, S. warnstorfii, S. rubellum and “conspecific” specimens, and S. venustum into different genetic clusters at K = 4, while the “conspecific” specimens form a fifth genetic cluster at K = 5 (Figure 3). Specimens of S. rubellum show varying extent of admixture with this cluster.

FIGURE 3.

FIGURE 3

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Barplots show the result of STRUCTURE analysis of 15 microsatellite data of five morphologically described Sphagnum sect. Acutifolia species and seven specimens assigned as conspecific. The order of the bars, from left to right, follows the order of individuals listed in Tables 1 and 2. The barplots show the results for different number of genetic clusters: 3 (results of 10/10 runs), 4 (results of 8/10) and 5 (10/10 runs). The PCoA (below) shows that S. venustum is separated from the other species, that are overlapping. The S. nitidulum sample (named and colored pink in the plot) was included as S. rubellum in the analysis and found within specimens of S. rubellum and S. capillifolium.

The results of the PCoA show that there is large variation within S. warnstorfii, S. rubellum, S. capillifolium, and the conspecific specimens, and that they overlap to some extent (Figures 3 and 4). Also, one individual of S. rubellum group with S. subnitens in the PCoA, but not in the Structure analysis (results not shown). Sphagnum venustum is clearly separated from the rest, and S. nitidulum is close to, but genetically distant from the bigger group of “red Acutifolia” (Figure 4). The distinctness of S. venustum and S. nitidulum is also evident the Neighbor‐Net network generated in SplitsTree (Figure 4). However, in the PCoA analysis of the “red Acutifolia” dataset, S. nitidulum is found within specimens of S. capillifolium and S. rubellum. In the network, specimens of S. subnitens, S. quinquefarium, S. beothuk, and S. fuscum group in their respective species, while S. warnstorfii, S. rubellum and S. capillifolium are not fully resolved, with occurrences in several places in the network. Also, the conspecific specimens are spread among S. rubellum and S capillifolium.

FIGURE 4.

FIGURE 4

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PCoA (left) generated in GenAlEx and Neighbor‐Net network (right) constructed in SplitsTree4, both based on genetic distance matrix calculated in GenAlEx6.501 of nine haploid Sphagnum species in subgenus Acutifolia and a group named “conspecific” that consists of specimens deviating morphologically and also somewhat genetically (see Structure results in Figure 3) from describe “red Acutifolia” species. Specimen ID in the network are the same as in Table 1, where voucher information is given.

4. DISCUSSION

Our findings seem to point to different paths leading to speciation in the subgenus Acutifolia. Sphagnum skyense is an example of instant speciation by polyploidization, a common speciation mode in Sphagnum (reviewed by Meleshko et al., 2018). We were able to identify the parents, which is not always possible (Kyrkjeeide et al., 2019; Kyrkjeeide, Hassel, Flatberg, Shaw, Yousefi, & Stenoien, 2016) as they may, for example, have gone extinct (Kyrkjeeide et al., 2019). Our genetical examination of S. skyense concludes that S. subnitens and S. quinquefarium are indeed the parental species. Sphagnum subnitens has two close relatives not included in the analyses: S. subfulvum Sjörs and S. flavicomans (Cardot.) Warnst. However, since they have been found to be genetically distinct based on microsatellite data (Kyrkjeeide et al., 2018), and S. subnitens and S. skyense mainly overlap in alleles, it is unlikely that either S. subfulvum or S. flavicomans are the parental species. Another allopolyploid species that has both parental species identified, is S. troendelagicum Flatberg (Såstad et al., 2001). Stenøien, Shaw, Stengrundet, and Flatberg (2011) estimated the origin of this species to about 40,000 years before present, indicating that the young age of the species make it possible to trace the parents. Both S. troendelagicum and S. skyense have narrow distribution ranges within areas glaciated during the last glacial maximum. Thus, S. skyense could have a recent origin like S. troendelagicum.

Genetic data show that S. venustum is a haploid species. Furthermore, it is genetically distinct from other similar Acutifolia species sharing the same habitat and geographical distribution range. Thus, we hypothesize that speciation may have taken place by niche differentiation along the mire structure gradient known in other Sphagnum species (Johnson et al., 2015).

Our PCoA result shows that S. nitidulum clusters within other ‘red Acutifolia’ species, but the haplotype is genetically distinct. We cannot conclude that it is a valid species based on our results, as a bigger sample size is needed to further explore whether it rather belongs to S. rubellum. Sphagnum rubellum is not with certainty collected from Terceira, and the included specimen collection of S. cf. rubellum shares its haplotype with S. nitidulum. The specimen of S. cf. rubellum from Terceira was collected in moist, sloping heath. As it is genetically identical to S. nitidulum, the genetic distinctness of the latter is likely not a result of adaptation to the sulfuric springs S. nitidulum is described from. A detailed morphological examination of the specimens was outside the scope of this study, but preliminary analysis indicate that the Azorean specimens collected as S. nitidulum and S. cf. rubellum are morphologically similar, further supporting no adaptation to an uncommon habitat. However, additional samples from Azores should be examined both morphologically and genetically to confirm which taxa occur at Terceira. Sphagnum warnstorfii is not reported from Terceira, but S. capillifolium is. It is necessary to study the phylogenetic relationship of the species to conclude on the validity of S. nitidulum, but also the origin of this taxon on Terceira. A larger selection of specimens from North America should be included in future analyses, as the Atlantic Ocean is a weak barrier to dispersal (Kyrkjeeide, Hassel, Flatberg, Shaw, Brochmann, & Stenoien, 2016; Stenøien et al., 2011).

The three red species, S. warnstorfii, S. capillifolium, and S. rubellum, form three distinct genetic groups, as expected (Shaw et al., 2005). However, the specimens collected as conspecific, group with S. rubellum, but overlap also with S. capillifolium and group close to S. warnstorfii in the PCoA. They have been identified as morphologically deviating, but conspecific to S. warnstorfii or S. capillifolium. Four specimens were collected as S. cf. capillifolium × warnstorfii, one was collected as S. cf. warnstorfii, and three more specimens were originally identified as S. warnstorfii, S. capillifolium and S. rubellum. A brief re‐examination of the morphology indicates that the conspecific group of specimens share characters and differ from other red Acutifolia, but a more thorough morphological examination and more genetic data should be included in a taxonomic revision to further explore this potential new taxon.

All three investigated taxa can be considered rare, since even though the amphi‐Atlantic S. venustum produces spores and has a wide distribution range, it seems to form very small populations where it occurs. It is only found at one site in Europe and assumed overlooked (Hallingbäck, 2019), and is assessed as data deficient in the European Red List of bryophytes (Hodgetts, Calix, et al., 2019). Both S. skyense and S. nitidulum, for the time being, are narrow endemics without known spore production, seemingly dependent upon fragmentation for dispersal. While S. nitidulum is evaluated in the IUCN global Red List of species as critically endangered (Gabriel & Sim‐Sim, 2019; Hodgetts, Calix, et al., 2019) due to the very small population size restricted to one site with declining habitat area, S. skyense occurs at several sites with no signs of decline and is thus evaluated as of least concern (Hodgetts, Calix, et al., 2019; Hodgetts, Lockhart, et al., 2019).

A morphological approach to describing species in the genus Sphagnum has proven useful, but due to large morphological variation along ecological gradients, like hight above water table, nutrient availability and light conditions, the determination of specimens can be very difficult both in the field and in the laboratory. Also, there is usually a time lag from the description of a new species until scientists and field biologist are reporting the species from new locations. Sphagnum skyense was described from Isle of Skye in 1988 (Flatberg, 1988a, 1988b), and then recorded again 16 years later. However, several new records were made the following years (Hill, 2014). All three species, but especially S. venustum and potentially S. nitidulum, should be searched for in mainland Europe. It could be that S. venustum has successfully established in Europe only once, but the species is small, with a somewhat dull color, and is therefore easy to overlook. The species is characterized morphologically (Flatberg, 2008) and included in floras (Flatberg, 2013; Laine et al., 2018), aiding field biologists with identification. On the other hand, if S. nitidulum is indeed a valid species, a morphological revision is needed to make it easier to distinguish it from other red Acutifolia species. In addition, a wider range of conspecific specimens should be investigated in terms of morphology, genetics, distribution ranges, and habitat preferences.

We have provided genetic data of three rare Sphagnum species with limited occurrences and assessments in Red lists. We have not studied intraspecific variation within these species, but found high genetic variation among the “red Acutifolia” species. Even though we were not able to fully resolve if S. nitidulum and the conspecific samples are genetically differentiated from S. rubellum, S. capillifolium, and S. warnstorfii, our findings indicate that there is genetic diversity within this group of species that should be prioritized for conservation. Ensuring protection of genetic variation safeguard biodiversity even in species groups where taxonomy is uncertain (Andrello et al., 2022; Rosauer et al., 2018). This is often the case for bryophyte species, where genetic diversity is not always expressed in identifiable morphological characters (Hedenäs, 2016), but is valid for all organisms groups were taxonomic work is limited due to high species diversity, few morphological characters or even lack of experts and taxonomists.

AUTHOR CONTRIBUTIONS

Magni Olsen Kyrkjeeide: Conceptualization (equal); data curation (equal); formal analysis (lead); methodology (lead); visualization (lead); writing – original draft (lead); writing – review and editing (lead). Olena Meleshko: Conceptualization (equal); data curation (supporting); formal analysis (supporting); methodology (supporting); writing – review and editing (equal). Kjell Ivar Flatberg: Conceptualization (equal); data curation (equal); writing – review and editing (equal). Kristian Hassel: Conceptualization (equal); data curation (supporting); methodology (supporting); writing – original draft (supporting); writing – review and editing (equal).

CONFLICT OF INTEREST STATEMENT

All authors declare that they have no conflicts of interest.

ACKNOWLEDGMENTS

Thanks to Line Birkeland at NINAGen for laboratory assistance. Thanks to three anonymous reviewers for valuable input.

Kyrkjeeide, M. O. , Meleshko, O. , Flatberg, K. I. , & Hassel, K. (2023). Short stories from Sphagnum of rare species, taxonomy, and speciation. Ecology and Evolution, 13, e10356. 10.1002/ece3.10356

DATA AVAILABILITY STATEMENT

The data are available in Table 2.

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Associated Data

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Data Availability Statement

The data are available in Table 2.

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