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Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa.

ABSTRACT: Lake expansion that leads to the formation of new habitats has potential to drive intralacustrine diversification. The ancient Lake Biwa in central Japan has historically experienced substantial changes in the lake size, and it provides a useful system for evaluating the role of lake-size fluctuations in the diversification of endemic fauna. Here, we used genome-wide DNA analyses and reconstructed the diversification history of the endemic freshwater snails belonging to the subgenus Biwamelania with respect to the geological history of Lake Biwa. We found that two genetically distinct snail lineages independently colonized Lake Biwa and they concurrently and rapidly radiated into 15 extant Biwamelania species. A combination of paleontological evidence and molecular dating technique demonstrated that the radiation of Biwamelania was tightly linked to the latest enlargement of the lake about 0.4 million years ago and suggested that increased ecological opportunity associated with the lake expansion drove the rapid adaptive radiation. We propose that the Biwamelania snails in Lake Biwa offer a promising new system for understanding the association between the geological history of the lake and rapid intralacustrine diversification.

SUBMITTER: Miura O

PROVIDER: S-EPMC6369999 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa.

Miura Osamu O Urabe Misako M Nishimura Tomohiro T Nakai Katsuki K Chiba Satoshi S

Evolution letters 20181130 1

Lake expansion that leads to the formation of new habitats has potential to drive intralacustrine diversification. The ancient Lake Biwa in central Japan has historically experienced substantial changes in the lake size, and it provides a useful system for evaluating the role of lake-size fluctuations in the diversification of endemic fauna. Here, we used genome-wide DNA analyses and reconstructed the diversification history of the endemic freshwater snails belonging to the subgenus <i>Biwamelan ...[more]

PMID: 30788141

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Project description:Background and aimsLake Biwa is one of the world's few ancient lakes. Formed ∼4 million years ago, the lake harbours many coastal species that commonly inhabit seashores. The beach pea Lathyrus japonicus is a typical coastal species of this freshwater lake, but its inland populations are faced with the threat of extinction. Here, we investigated the phylogeographical and population structures of both inland and coastal populations of L. japonicus. We also elucidated the historical isolation of the Lake Biwa population.MethodologyIn total, 520 individuals from 50 L. japonicus populations were sampled throughout the species distribution in Japan. Chloroplast haplotyping using intergenic spacers psbA-trnH and atpI-atpH was performed to investigate the phylogeographical structure as well as the genetic diversity of L. japonicus. Six nuclear microsatellite markers were also used to analyse the population structure.Principal resultsPopulation structure analyses of chloroplast DNA (cpDNA) and nuclear DNA (nDNA) identified inland and coastal groups. Based on the genetic differentiation, inland populations exhibited a single cpDNA haplotype and significantly lower values of H(S), AR and F(IS) than coastal populations. In addition to the presence of a bottleneck, the lack of gene flow among inland populations was supported by estimates of recent migration rates between subpopulations.ConclusionsOur data revealed that inland populations have been isolated in Lake Biwa as 'landlocked' populations since the predecessor lake was isolated from sea. This was also seen in a previous study of Calystegia soldanella. However, the high genetic differentiation, accompanied by a lack of gene flow among the Lake Biwa populations (according to the BAYESASS(+) analysis), contradicts the results with C. soldanella. We conclude that because of the presence of a bottleneck and low genetic diversity of the inland populations, self-sustaining population persistence may be difficult in the future. Conservation strategies must consider the genetic properties of such isolated populations.

Dataset Information

Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa.

Publications

Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa.

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