Diversification in ancient Lake Biwa: integrative taxonomy reveals overlooked species diversity of the Japanese freshwater snail genus Semisulcospira (Mollusca: Semisulcospiridae)

Abstract

The freshwater snail genus Semisulcospira has adaptively radiated in the ancient Lake Biwa, Japan. Although significant geographical variations have been known in the shell morphology of Semisulcospira niponica, their systematics remain uncertain. We evaluated the systematic status of the geographical variations in S. niponica and its congenerics S. biwae and S. fuscata through morphological and genetic investigations. Genome-wide snp s were used to estimate their genetic relationships. Random Forest algorithms explored the morphological variation of the shells of the name-bearing types and newly collected specimens. Our results detected five genetic clusters and revealed the consistency of adult shell morphology with genetic relationships, reinforcing the robustness of shell morphology-based species delimitation of the genus. The present systematics synonymized S. biwae under S. niponica. The five genetic clusters corresponded to the two described species, S. niponica and S. fuscata, and three new species, Semisulcospira watanabei sp. nov., Semisulcospira nakanoi sp. nov., and Semisulcospira salebrosa sp. nov. discovered among the geographical variations of S. niponica. The observed similarities in substrate preference and differences in distribution patterns among species suggest that the diversification of the genus was accelerated by geographical isolation after the initial ecological niche differentiation. We suggest that the distributions of Semisulcospira species may have been influenced by competitive exclusion among them, and that multiple speciation events have occurred in similar patterns.

Systematic revision of the Japanese freshwater snail

“…nov. on the different substrates. The previous phylogenetic study supported morphology-based species delimitation in the genus (Miura et al 2019), and the characteristics of the teleoconch discriminated closely related genetic clusters better than the protoconch and radula (Sawada and Fuke 2022). In contrast, this was not the case for the present species.…”

“…The present investigation found that S. decipiens and S. arenicola are widely distributed in Lake Biwa across different substrates, while their sympatric occurrences with closely related species are restricted at several sites. Semisulcospira niponica and its relatives infrequently form sympatric distributions, suggesting the possibility of species-specific microhabitat differences or competitive exclusion (Sawada and Fuke 2022). These factors may also contribute to distributional patterns among the species examined in this study.…”

“…The karyotypic relationships among the species strongly corresponded with the present genetic results. Karyotypes of most of the lacustrine species were reported by Burch and Davis (1967) Hybridization may occur infrequently in the lacustrine Semisulcospira, as suggested by Sawada and Fuke (2022). This is because the putative hybrids were only found at the boundary between the parapatric distribution of S. arenicola and S. nakasekoae.…”

“…Past genetic introgression and insufficient variation in the allozyme loci have hampered the clarification of their phylogenetic relationships (Kamiya et al 2011;Köhler 2016;Miura et al 2020). However, recent genome-wide SNP analyses have shown that the previous shell morphology-based species delimitation is concordant with the nuclear phylogeny (Miura et al 2019;Sawada and Fuke 2022).…”

“…Those comparative studies have established taxonomic diagnoses for the lacustrine species. However, the recent revision of the type specimens has also amended accounts of several older species described in the 1800s Sawada and Fuke 2022). Broad sampling and genetic analyses have also been used to identify new species from a geographic variation of the known species.…”