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. 2024 Mar 5;24(2):4. doi: 10.1093/jisesa/ieae028

Mitochondrial genomes of Nemourinae species (Plecoptera: Nemouridae) and the phylogenetic implications

Ying Wang 1,✉, Caiyue Guo 2, Xiaoxiao Yue 3, Xing Fan 4, Yuying Fan 5, Jinjun Cao 6
Editor: Ren-Huai Dai
PMCID: PMC10914373  PMID: 38442353

Abstract

Currently, the classification system of 2 subfamilies within Nemouridae has been widely accepted. However, monophyly of 2 subfamilies has not been well supported by molecular evidence. To date, only mitogenomes from genus Nemoura of the subfamily Nemourinae were used in previous phylogenetic studies and produced conflicting results with morphological studies. Herein, we analyzed mitogenomes of 3 Nemourinae species to reveal their mitogenomic characteristics and to examine genus-level classification among Nemouridae. In this study, the genome organization of 3 mitogenomes is highly conserved in gene order, nucleotide composition, codon usage, and amino acid composition. In 3 Nemourinae species, there is a high variation in nucleotide diversity among the 13 protein-coding genes (PCGs). The Ka/Ks values for all PCGs were far lower than 1, indicating that these genes were evolving under purifying selection. The phylogenetic analyses highly support Nemurella as the sister group to Ostrocerca. Meanwhile, Nemoura is recovered as the sister group of Malenka; they are grouped with other Amphinemurinae and emerged from a paraphyletic Nemourinae. More molecular data from different taxonomic groups are needed to understand stoneflies phylogeny and evolution.

Keywords: Plecoptera, Nemourinae, mitochondrial genome, phylogeny

Introduction

Plecoptera, commonly known as stoneflies, is an ancient group of insects with fossil records dating back to the Triassic period (Zwick 2000, DeWalt et al. 2023). There are over 4,000 known species of stoneflies worldwide, distributed across most continents, with the exception of Antarctica (Zwick 2000, DeWalt et al. 2023). Stoneflies are particularly abundant in regions with cooler, clean mountain streams and rivers (Zwick 2000). Their nymphs are sensitive to changes in water quality and habitat health, making them valuable bioindicators for monitoring freshwater ecosystems (Fochetti and Figueroa 2008, Stewart and Stark 2008, Qian et al. 2014).

Nemouridae species are commonly known as spring stoneflies due to their emergence in late winter and early spring. It is one of the largest families of Plecoptera with over 600 species founded worldwide (DeWalt et al. 2023). For a long time, the classification system of Nemouridae has been in constant flux. Newman (1853) first erected Nemouridae and included most of the present Euholognatha in this family. Later, this large diverse grouping was divided into 5 families of the present superfamily Nemouroidea (Klapálek 1905, Zwick 1973). After revising most of the genera of Nemouridae, Baumann (1975) divided this family into 2 subfamilies (Nemourinae and Amphinemurinae) and 17 genera. Recently, 4 more genera (Sphaeronemoura, Tominemoura, Nanonemoura, and Sinonemura) have been added, bringing the total number of genera in this family to 21 (Baumann and Fiala 2001, Shimizu and Sivec 2001, Sivec and Stark 2009, Mo et al. 2020). Although Baumann (1975) proposed a widely accepted classification system for the family Nemouridae based on morphological data, the monophyly of 2 subfamilies has not been well supported by molecular evidence, and conflicting results have been produced (Terry and Whiting 2003, Gamboa et al. 2019, South et al. 2021).

Insect mitochondrial genomes (mitogenomes) are of particular interest to biologists due to their compact size, rapid evolution, and unique genetic features, making them useful tools for studying comparative and evolutionary genomics, phylogenetics, and population genetics (Wilson et al. 2000, Lin and Danforth 2004, Gissi et al. 2008, Salvato et al. 2008, Cameron 2014).

To date, there are 9 complete or nearly complete Nemourinae mitogenomes available in the NCBI database (Table 1). Most mitogenomes were from species of the genera Nemoura, whereas only 2 of them were from genus Nemurella and Lednia. For those Nemourinae mitogenomes, only mitogenomes from genus Nemoura were used in previous phylogenetic studies because of an unannotated sequence of Nemurella pictetii (GenBank accession no. OV121127) and an uncompleted sequence of Lednia tumana (GenBank accession no. MH374046). Most of these studies proposed a sister group of Nemoura and Amphinemura, leading a paraphyletic Amphinemurinae (Chen and Du 2017a, 2017b, Cao et al. 2019, 2021, Chen et al. 2020, Guo et al. 2022). Therefore, to obtain a more precise phylogenetic relationship, it is necessary to incorporate mitogenomic data, especially the data from other genera of Nemourinae.

Table 1.

Species used for phylogenetic analyses in this study.

Subfamily Species Length Accession number
Nemourinae Nemoura avicularis 15,590 MT410776a
Nemoura cinerea 15,640 MT410849a
Nemoura flexura 15,780 MT584119a
Nemoura longicercia 15,728 OM287982
Nemoura meniscata 15,895 MN944386
Nemoura nankinensis 16,602 KY940360
Nemoura papilla 15,774 MK290826
Nemurella pictetii 15,934 OR601702
Lednia tumana 15,294 OR601701a
Ostrocerca truncata 15,971 OR398225
Amphinemurinae Amphinemura bulla 15,827 MW339348
Amphinemura claviloba 15,707 MN720741
Amphinemura longispina 15,709 MH085446
Amphinemura sp. 15,176 KX091847a
Amphinemura yao 15,876 MH085447
Indonemoura auriformis 15,718 MN419915
Indonemoura jacobsoni 15,642 MH085448
Indonemoura nohirae 15,738 NC_044751
Malenka flexura 15,744 ON411527
Mesonemoura metafiligera 15,739 MH085450
Mesonemoura tritaenia 15,778 MH085451
Protonemura datongensis 15,756 MT276842
Protonemura kohnoae 15,707 MH085452
Protonemura meyeri 15,695 NC_050322
Protonemura orbiculata 15,758 MH085453
Sphaeronemoura acutispina 15,016 MH085455a
Sphaeronemoura elephas 15,846 MN944385
Sphaeronemoura grandicauda 15,661 MH085454
Sphaeronemoura hainana 15,260 MK111420a
Perlidae (outgroups) Caroperla siveci 15,353 MG677942a
Kamimuria klapaleki 16,077 MN400755
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aNearly complete genome sequence.

In this study, we sequenced the complete mitogenome of Ostrocerca truncata and completed the missing rRNA sequences in L. tumana mitogenome. In addition, we annotated the mitogenome of N. pictetii for further analysis. We characterized and compared the mitogenomes of these 3 Nemourinae species and revealed mitogenomic characterizations of this subfamily in the present study for the first time. Finally, phylogenetic analysis is provided to evaluate feasibility of mitogenome data to resolve relationships at the genus level in Nemouridae.

Materials and Methods

Sample Collection and DNA Extraction

Specimens of O. truncata were collected from Hidden Valley, Virginia. Specimens were soaked in 100% ethanol and stored at −20 °C. Total genomic DNA was extracted from muscle tissue using the DNeasy Extraction kit (Qiagen, Germany), according to the manufacturer’s instructions.

Genome Sequencing, Assembly, and Annotation

Mitogenomes were sequenced and assembled as described in our previous studies (Wang et al. 2018a, 2018b, 2019, Cao et al. 2019, 2021). Genomic DNA with qualified concentration was submitted to Berry Genomics Co., Ltd. (Beijing, China) for library construction and high-throughput sequencing. An Illumina TruSeq library with an average insert size of 350 bp was generated and sequenced with 150 bp paired-end reads on the Illumina Hiseq 2500 platform. The mitogenome was assembled using Trimmomatics v0.30 (Lohse et al. 2012) and IDBA-UD (Peng et al. 2012). MitoZ was used to annotate the obtained mitogenome (Meng et al. 2019).

The transfer RNA (tRNA) genes of O. truncata were identified by using the MITOS Web Server (Bernt et al. 2013). Protein-coding genes (PCGs) and 2 ribosomal RNA (rRNA) genes were identified by alignment with homologous genes from other published stonefly mitogenomes. Base composition and codon usage were analyzed by MEGA v.6.0 (Tamura et al. 2013). Composition skew analysis was carried out with the formulas AT skew = [A − T]/[A + T] and GC skew = [G − C]/[G + C], respectively (Perna and Kocher 1995).

Phylogenetic Analysis

Phylogenetic analysis was carried out based on the 30 complete or nearly complete mitogenomes from the family Nemouridae. Two species (Kamimuria klapaleki and Caroperla siveci) from Perlidae were selected as outgroups (Table 1). Each PCG was individually aligned using the MAFFT algorithm (Katoh and Standley 2013) within the TranslatorX online platform (Abascal et al. 2010). Two rRNA genes were independently aligned with the MAFFT online service with G-INS-i strategy (Katoh and Standley 2013), and unreliably aligned regions were removed using Gblocks (Talavera and Castresana 2007). One dataset was concatenated for phylogenetic analyses: PCG12R matrix, including the first and second codon positions of the 13 PCGs and 2 rRNAs (9,490 bp).

Bayesian inference (BI) and maximum likelihood (ML) analysis were conducted using MrBayes 3.2.6 (Ronquist et al. 2012) and IQ-TREE web server (Trifinopoulos et al. 2016), respectively. The best-fit model of nucleotide sequences for ML and BI method was selected by ModelFinder (Trifinopoulos et al. 2016), and the GTR + I + G model was optimal for analysis with nucleotide alignments according to the Akaike information criterion. For BI analyses, 2 simultaneous runs of 10 million generations were performed for each dataset, and trees were sampled every 1,000 generations, with a burn-in rate of 25%. For ML analyses, phylogenetic trees were conducted using an ultrafast bootstrap approximation with 1,000 replicates.

Results and Discussion

Mitogenome Organization and Base Composition

The complete mitogenomes of O. truncata and N. pictetii are 15,971 and 15,934 bp in size, respectively (Fig. 1, Table 1). The partial mitogenome of L. tumana is 15,294 bp in length (Fig. 1, Table 1). The length of completely sequenced mitogenomes was medium sized when compared with the mitogenomes of other nemourid species (Table 1). Differences in gene length among 3 Nemourinae species were primarily caused by insertions/deletions in the intergenic spacers and control region (Supplementary Tables S1–S3). The gene order of 3 Nemourinae mitogenomes is the same as all previously published stonefly mitogenomes 22–30 (Chen and Du 2017a, 2017b, Wang et al. 2017, 2021, Cao et al. 2019, 2021, Chen et al. 2020, Zhao et al. 2020, Guo et al. 2022), as well as the ancestral gene order of Drosophila yakuba (Clary and Wolstenholme 1985).

Fig. 1.

Fig. 1.

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Mitochondrial genome maps of Ostrocerca truncata, Nemurella pictetii, and Lednia tumana. Genes shown on the inside of the map are transcribed in a clockwise direction, whereas those on the outside of the map are transcribed counterclockwise. Different gene types are shown as filled boxes in different colors.

There are 10, 11, and 10 intergenic spacers in the mitogenomes of O. truncata, N. pictetii, and L. tumana, respectively, ranging in size from 1 to 137 bp (Supplementary Tables S1–S3). The longest (137 bp) intergenic spacer was located between tRNASer(UCN) and ND1 in N. pictetii (Supplementary Table S3). At the same region, the lengths of the intergenic spacer are 36 and 20 bp in O. truncata and L. tumana, respectively (Supplementary Tables S1 and S2). There are 12, 13, and 14 gene overlaps in the mitogenomes of O. truncata, N. pictetii, and L. tumana, respectively, ranging from 1 to 8 bp in length (Supplementary Tables S1–S3).

The nucleotide composition of 3 Nemourinae mitogenomes is significantly biased toward A and T, ranging from 66.9% in L. tumana to 71.8% in O. truncata (Table 2). Among the 4 partitions in 2 complete mitogenomes of O. truncata and N. pictetii, the control region has the highest A + T content value (82.4% and 85.8%), followed by rRNAs (73.5% and 73.2%), tRNAs (71.6% and 71.5%), and PCGs (70.7% and 68.7%). Similarly, the high A + T content value among the 3 partitions also occurs in the partial mitogenome of L. tumana (Table 2). As with published stoneflies (Chen and Du 2017a, 2017b, Wang et al. 2017, 2021, Cao et al. 2019, 2021, Chen et al. 2020, Zhao et al. 2020, Guo et al. 2022) and other insects (Wei et al. 2010a), all 3 species showed a positive AT-skew and negative GC-skew in the whole mitogenome (Table 2).

Table 2.

Nucleotide composition of the mitogenomes of Ostrocerca truncate, Lednia tumana, and Nemurella pictetii

O. truncate L. tumana N. pictetii
Full mitogenome Size 15,971 15,294 15,934
AT% 71.8 66.9 70.7
AT skew 0.03 0.07 0.04
GC skew −0.16 −0.21 −0.19
13PCGs Size 11,232 11,235 11,232
AT% 70.7 65.0 68.7
tRNAs Size 1,460 1,471 1,471
AT% 71.6 71.1 71.5
rRNAs Size 2,131 2,120 2,126
AT% 73.5 72.5 73.2
Control region Size 1,047 >462 969
AT% 82.4 — 85.5
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There are 22 traditional tRNAs, which ranged from 63 to 71 bp in the 3 mitogenomes (Supplementary Tables S1–S3). All tRNAs can be folded into the typical clover-leaf structure with the exception of tRNASer(AGN) due to the lack of a stable dihydrouridine (DHU) arm. Like other published stoneflies (Wang et al. 2017, 2021, Cao et al. 2019, 2021, Chen et al. 2020, Guo et al. 2022), the anticodon stem of tRNASer(AGN) in 3 mitogenomes has an extended nucleotide (9 pairs of nucleotides) (Fig. 2). Five types of mismatched base pairs (G-U, A-A, A-C, A-G, and C-U) are revealed in the tRNA secondary structures of 3 mitogenomes. These unmatched base pairs might be corrected by RNA editing without leading to obstruction in amino acid transportation (Bae et al. 2004). As in most other insect mitogenomes, the large (lrRNA or 16S) and small (srRNA or 12S) ribosomal RNAs in 3 Nemourinae species are located between tRNALeu(CUN) and tRNAVal, and tRNAVal and the control region, respectively (Fig. 1).

Fig. 2.

Fig. 2.

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Inferred secondary structure of tRNASer (AGN) in 3 Nemourinae mitogenomes.

The mitochondrial control region is located between lrRNA and tRNAIle and is suggested to act on the initiation and regulation of insect replication and transcription (Sheffield et al. 2008, Wei et al. 2010b). The control region of O. truncata and N. pictetii is 1,047 and 969 bp, respectively (Supplementary Tables S1 and S3). However, the control region of L. tumana has not been entirely sequenced, with a measured length of 462 bp in this study (Supplementary Table S2).

Protein-Coding Genes

The total lengths of 13 PCGs are 11,232, 11,235, and 11,232 bp, respectively (Table 2). Among 3 Nemourinae mitogenomes, most PCGs initiate with ATN as the start codon. However, ND1 in 3 species uses TTG as the start codon, and ND5 in O. truncata and N. pictetii use GTG as the start codon (Supplementary Tables S1–S3). These unconventional start codons are also used in some species to minimize intergenic spacer and avoid overlap with adjacent genes (Ojala et al. 1981, Yokobori and Pääbo 1995, Cha et al. 2007). Most PCGs employ the complete termination codons TAA or TAG, whereas COII and ND5 in 3 species have incomplete stop codon T (Supplementary Tables S1–S3). The presence of an incomplete stop codon is common in insect mitogenomes, and it has been presumed that the complete stop codon TAA can be generated through post-transcriptional polyadenylation (Zhang et al. 1995, Zhang and Hewitt 1997).

The relative synonymous codon usage of the 3 Nemourinae mitogenomes is summarized in Fig. 3. The codons ending with A or U are preferred to both the 4- and 2-fold degenerate codons (Fig. 3). The 4 most commonly used amino acid codons, UUA (Leu1), UUU (Phe), AUU (Ile), and AUA (Met), are all exclusively composed of A and/or U (Fig. 4).

Fig. 3.

Fig. 3.

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Relative synonymous codon usage in 3 Nemourinae mitogenomes.

Fig. 4.

Fig. 4.

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Amino acid composition in 3 Nemourinae mitogenomes.

In 3 Nemourinae species, there is a high variation in nucleotide diversity among the 13 PCGs, with values ranging from 0.132 (ATP8) to 0.286 (ND6). The gene ATP8 (Pi = 0.132) has the lowest value of nucleotide diversity among all PCGs and is the most conserved gene. In contrast, ND6 (Pi = 0.286) has the highest value of nucleotide diversity and is the most variable gene (Fig. 5).

Fig. 5.

Fig. 5.

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Nucleotide diversity (Pi) and nonsynonymous (Ka) to synonymous (Ks) substitution rate ratios of 13 protein-coding genes of 3 Nemourinae species. The Pi and Ka/Ks values of each PCGs shown under the gene name.

To investigate evolutionary patterns of PCGs, the nonsynonymous (Ka)/synonymous (Ks) substitution rate ratios for each PCG were calculated (Fig. 5). The COI and ND6 exhibit the lowest (0.033) and highest (0.290) evolutionary rates, respectively. However, the Ka/Ks values for all PCGs are lower than 1, indicating that they are evolving under the purifying selection and are suitable for investigating phylogenetic relationships within the Nemourinae.

Phylogenetic Analyses

In this study, the ML and BI analyses based on the PCG12R matrix generated the phylogenic trees with same topologies and high nodal supports (Fig. 6). In the 2 analyses, relationships of 5 genera in Amphinemurinae were recovered as follows: (((Sphaeronemoura + Mesonemoura) + Indonemoura) + Protonemura) + Amphinemura. In addition, the monophyly of Nemourinae and Amphinemurinae was not recovered. Nemoura was recovered as the sister group of Malenka, and they were grouped with other Amphinemurinae and emerged from a paraphyletic Nemourinae. Relationships of the other 3 genera in Nemourinae were recovered as ((Nemurella + Ostrocerca) + Lednia).

Fig. 6.

Fig. 6.

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Phylogenetic tree of the 31 sequenced stoneflies. BI and ML analyses inferred from PCG12R matrix supported the same topological structure. Values at nodes are Bayesian posterior probabilities and ML bootstrap values. The tree was rooted with 3 outgroups.

Baumann (1975) first studied the genus-level phylogenetic relationships within Nemouridae using morphological data, confirming the monophyly of 2 subfamilies. Subsequent research has mainly focused on describing and identifying new species and genera, without further investigation into the phylogenetic relationships within Nemouridae. Currently, most molecular studies have failed to support the monophyly of the subfamily Amphinemurinae (Terry and Whiting 2003, Zhao et al. 2020, Cao et al. 2021, Wang et al. 2021, Guo et al. 2022). Previous morphological study supported Amphinemura and Malenka as a sister group (Baumann 1975). However, it was not supported by early molecular studies (Thomas et al. 2000, Terry and Whiting 2003) and our previous mitochondrial study (Cao et al. 2022). Although our results still do not support the sister relationships between Amphinemura and Malenka, the relationships among the remaining 4 genera are consistent with the traditionally proposed relationships (Baumann 1975) and previous studies (Cao et al. 2019, 2021, Wang et al. 2021).

In our analyses, the sister group relationship between Nemurella and Ostrocerca was supported, and then they were grouped with Lednia. This result is consistent with that of morphological hypothesis (Baumann 1975). Although the monophyly of Nemourinae was not recovered, the mitogenome from Ostrocerca allows us to have a more comprehensive understanding of its phylogenetic relationships among Nemourinae for the first time. Apart from Amphinemura and Nemoura, which are widely distributed in the Nearctic, Palearctic, and Oriental regions, the majority of genera within Nemouridae are endemic to either the Oriental and Palearctic regions or the Nearctic region (Baumann 1975, DeWalt et al. 2023). It will also be extremely helpful to study and assign the species placed in incertae sedis to their proper places in the phylogenetic scheme (Baumann 1975). These 3 genera belong to the subfamily Nemourinae, but all of them are only distributed in North America. Maybe it can be explained by animal geography. However, due to the limitations of mitochondrial genes, their relationship is still unclear, and more gene sequencing is necessary to explore this problem.

Supplementary Material

ieae028_suppl_Supplementary_Tables_S1-S3
ieae028_suppl_supplementary_tables_s1-s3.docx (33.3KB, docx)

Acknowledgments

This research was funded by the National Natural Science Foundation of China (31801999; 32270492), the Program for Science & Technology Innovation Talents in Universities of Henan Province (21HASTIT042), and the Key Scientific Research Project of Henan Province (22A210004).

Contributor Information

Ying Wang, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Caiyue Guo, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Xiaoxiao Yue, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Xing Fan, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Yuying Fan, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Jinjun Cao, Department of Plant Protection, Henan International Joint Laboratory of Taxonomy and Systematic Evolution of Insecta, Henan Institute of Science and Technology, Hualan Road, Xinxiang 453003, China.

Author Contributions

Ying Wang (Conceptualization [Equal], Data curation [Lead], Formal analysis [Equal], Funding acquisition [Equal], Investigation [Equal], Writing—original draft [Equal], Writing—review & editing [Equal]), Caiyue Guo (Formal analysis [Equal], Investigation [Equal], Writing—original draft [Equal]), Xiaoxiao Yue (Formal analysis [Equal], Investigation [Equal]), Xing Fan (Formal analysis [Equal], Investigation [Equal]), Yuying Fan (Investigation [Equal]), and Jinjun Cao (Conceptualization [Equal], Funding acquisition [Equal], Writing—review & editing [Equal])

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