Systematic revision of the freshwater snailMargarya Nevill, 1877 (Mollusca: Viviparidae) endemic to the ancient lakes of Yunnan, China, with description of new taxa

Abstract

The systematics of the viviparid freshwater snail genus Margarya endemic to the ancient lakes of Yunnan, China, is revised based on comparative analyses of morphological features, including shell, operculum, radula, and genital anatomy, and molecular phylogenetic analyses of partial sequences of the mitochondrial 16S rDNA (16S) and cytochrome c oxidase subunit I (COI) genes, as well as the nuclear Internal Transcribed Spacer 2 (ITS2). The taxonomic utility of key anatomical and morphological features in this group is evaluated. The genus Margarya as delimited previously is split into three genera in order to retain monophyletic taxa: (1) Margarya s.s., consisting of four species, i.e. the type species Margarya melanioides plus Margarya francheti, Margarya oxytropoides, and Margarya monodi; (2) the previously introduced subgenus Tchangmargarya is elevated to an independent genus containing two species, Tchangmargarya yangtsunghaiensis and the new species Tchangmargarya multilabiata sp. nov.; and (3) a new genus, Anularya gen. nov., is described, also containing two species, i.e. Anularya mansuyi and Anularya bicostata. Molecular phylogenies based on analyses of three gene fragments have identical topologies, supporting the monophyly of these genera. The sister group of Margarya s.s. is Cipangopaludina, whereas the sister group of Anularya is Sinotaia; Tchangmargarya is sister to a clade containing all the aforementioned groups. Features of the operculum and the right male tentacle (penis) are particularly informative on the generic level, whereas shell and radular characters are especially useful to differentiate species. The phylogenetic relationships recovered here are consistent with orogenic patterns of the Yunnan Mountains. Changes in the river system and water area of ancient lakes caused by tectonic activities probably play an important role in speciation and shaping the current pattern of species distribution in Yunnan.

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

“…Numbers on the maps correspond with node numbers of Figure . Distributions of widely distributed genera Cipangopaludina , Sinotaia , and Mekongia in clade A are not included in maps b and c. Distributions are based on Starobogatov Prozorova Bogatov and Saenko (), Anistratenko Degtyarenko Anistratenko and Prozorova (), Prozorova et al (), Hirano et al (), Hirano et al (), Zhang et al (), and Van Bocxlaer et al (). [Colour figure can be viewed at wileyonlinelibrary.com]…”

“…There are some ancient lakes in East and Southeast Asia that are hotspots of species diversity (Miura et al, ; Strong, Gargominy, Ponder, & Bouchet, ; Zhang, Chen, Yang, Jin, & Köhler, ). For example, Yunnan Province (Southwest China) has multiple ancient lake groups (e.g., Lakes Dianchi, Fuxian, Xingyun, and Qilu).…”

“…Lakes Fuxian, Xingyun and Qilu are the remains of a large palaeolake (the Great Fuxian Palaeolake), which formed about 3.4 Ma (Wang & Dou, ). These lakes harbour a unique fauna of at least 241 fish and 124 gastropod species, most of which are endemic to the region (Chu & Chen, ; Zhang et al, , ). In Japan, ancient Lake Biwa also harbours rich fauna and flora (>1,000 species/subspecies), including ~60 endemic species/subspecies (Nishino, ; Nishino & Hamabata, ).…”

“…In the present study, we focused on the freshwater snail family Viviparidae (Gray, 1847), which is endemic to all continents, except Antarctica and South America (Brown, ; Van Bocxlaer, Strong, Richter, Stelbrink, & von Rintelen, ); also absent from New Zealand and Madagascar and includes ~150 species and 31 genera which are considered valid (Strong et al, ). Many endemic species of Viviparidae are diversified in ancient lakes (e.g., Africa: Schultheiß, Van Bocxlaer, Riedel, von Rintelen, & Albrecht, ; Sengupta, Kristensen, Madsen, & Jørgensen, ; Southwest China: Du, Yang, von Rintelen, Chen, & David, ; Zhang et al, ; Japan: Hirano, Saito, & Chiba, ). In the case of Asian viviparid snails, Du et al () reported that the genus Margarya , endemic to the ancient lake groups in Yunnan Province, was polyphyletic.…”

“…Molecular phylogenomics using a multilocus approach provides more detailed information than a single or a few genes (Razkin et al, ; Rivers, Darwell, & Althoff, ; Rubinoff & Holland, ; Takahashi & Moreno, ). Although prior studies focusing on phylogenetic relationships among viviparid species were performed using only a few genes (Du et al, ; Gu et al, ; Hirano et al, ; Schultheiß et al, ; Sengupta et al, ; Van Bocxlaer et al, ; Zhang et al, ) or mtDNA genome (Wang, Zhang, Jakovlić, & Wang, ), our previous study indicated that genome‐wide single nucleotide polymorphism (SNP) was more useful for clarifying the relationships and population demographic history between viviparid species (Hirano et al, ).…”