Enigmatic incongruence between mtDNA and nDNA revealed by multi-locus phylogenomic analyses in freshwater snails

Abstract

Phylogenetic incongruence has frequently been encountered among different molecular markers. Recent progress in molecular phylogenomics has provided detailed and important information for evolutionary biology and taxonomy. Here we focused on the freshwater viviparid snails ( Cipangopaludina chinensis chinensis and C. c. laeta ) of East Asia. We conducted phylogenetic analyses and divergence time estimation using two mitochondrial markers. We also performed population genetic analyses using genome-wide SNPs. We investigated how and which phylogenetic patterns reflect shell morphology. The results showed these two species could be separated into four major mitochondrial clades, whereas the nuclear clusters supported two groups. The phylogenetic patterns of both mtDNA and nDNA largely reflected the geographical distribution. Shell morphology reflected the phylogenetic clusters based on nDNA. The findings also showed these two species diversified in the Pliocene to early Pleistocene era, and occurred introgressive hybridisation. The results also raise the taxonomic issue of the two species.

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]…”

“…To obtain genome‐wide SNP information of these species groups from total DNA, we conducted MIG‐seq method (Suyama & Matsuki, ). MIG‐seq is a type of reduced representation sequencing such as restriction site‐associated DNA sequencing, and especially effective for low‐quality DNA and small quantities of DNA (Tamaki, Yoichi, Matsuki, Suyama, & Mizuno, ), which was performed for viviparid snails in previous research (Hirano et al, ). Preparation of the MIG‐seq library was executed under a method modified from Suyama and Matsuki () using an Illumina MiSeq Sequencer (Illumina), and an MiSeq Reagent Kit version 3 (150 cycle; Illumina) (Hirano et al, ; Y. Tsunamoto et al, unpublished data).…”

“…In Japan, modern viviparid fauna comprises five species in three genera (Hirano et al, , ). One of these, Cipangopaludina japonica (Martens, 1861) is widely distributed in mainland Japan freshwater ecosystems, including ponds, gentle streams, and lake habitats.…”

“…In viviparid snails there are some taxonomic issues. For example, the type species of Cipangopaludina , Hannibal, 1912 is C. malleata (Reeve, 1863) described as from Japan, but the detailed type locality of C. malleata was not identified in the description (Hirano et al, ). Habe (), Pilsbry (), and Ponder, Hallan, Shea, and Clark () suggested that this species is synonymous with C. laeta (Martens, 1861) or C. chinensis (Gray, 1834).…”

“…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, ).…”