Sequencing of the complete mitochondrial genomes of eight freshwater snail species exposes pervasive paraphyly within the Viviparidae family (Caenogastropoda)

PLoS One. 2017 Jul 25;12(7):e0181699. doi: 10.1371/journal.pone.0181699. eCollection 2017.

Abstract

Phylogenetic relationships among snails (Caenogastropoda) are still unresolved, and many taxonomic categories remain non-monophyletic. Paraphyly has been reported within a large family of freshwater snails, Viviparidae, where the taxonomic status of several species remains questionable. As many endemic Chinese viviparid species have become endangered during the last few decades, this presents a major obstacle for conservation efforts. Mitochondrial genomes (mitogenomes) carry a large amount of data, so they can often provide a much higher resolution for phylogenetic analyses in comparison to the traditionally used molecular markers. To help resolve their phylogenetic relationships, the complete mitogenomes of eight Chinese viviparid snails, Viviparus chui, Cipangopaludina chinensis, C. ussuriensis, C. dianchiensis (endangered), Margarya melanioides (endangered), M. monodi (critically endangered), Bellamya quadrata and B. aeruginosa, were sequenced and compared to almost all of the available caenogastropod mitogenomes. Viviparidae possess the largest mitogenomes (16 392 to 18 544 bp), exhibit the highest A+T bias (72.5% on average), and some exhibit unique gene orders (a rearrangement of the standard MYCWQGE box), among the Caenogastropoda. Apart from the Vermetidae family and Cerithioidea superfamily, which possessed unique gene orders, the remaining studied caenogastropod mitogenomes exhibited highly conserved gene order, with minimal variations. Maximum likelihood and Bayesian inference analyses, used to reconstruct the phylogenetic relationships among 49 almost complete (all 37 genes) caenogastropod mitogenomes, produced almost identical tree topologies. Viviparidae were divided into three clades: a) Margarya and Cipangopaludina (except C. ussuriensis), b) Bellamya and C. ussuriensis, c) Viviparus chui. Our results present evidence that some Cipangopaludina species (dianchiensis and cathayensis) should be renamed into the senior genus Margarya. The phylogenetic resolution obtained in this study is insufficient to fully resolve the relationships within the 'b' clade, but if C. chinensis proves to be a valid representative of the genus, C. ussuriensis may have to be reassigned a different genus (possibly Bellamya, or even a new genus). Non-monophyly also remains pervasive among the higher (above the family-level) Caenogastropod taxonomic classes. Gene order distance matrix produced a different phylogenetic signal from the nucleotide sequences, which indicates a limited usability of this approach for inferring caenogastropod phylogenies. As phenotypic homoplasy appears to be widespread among some viviparid genera, in order to effectively protect the rapidly diminishing endemic Viviparid populations in China, further detailed molecular phylogenetic studies are urgently needed to resolve the taxonomic status of several species.

MeSH terms

  • Animals
  • China
  • Gastropoda / classification
  • Gastropoda / genetics*
  • Genome, Mitochondrial / genetics*
  • Phylogeny
  • Polymerase Chain Reaction
  • Sequence Analysis, DNA

Grants and funding

This study was supported by the two major Chinese "National Water Pollution Control and Management Technology" Projects: 2012ZX07203-006 and 2014ZX07203010-4. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.