Phylogeny and historical demography of endemic fishes in Lake Biwa: the ancient lake as a promoter of evolution and diversification of freshwater fishes in western Japan

Abstract

To elucidate the origins of the endemic fish of Lake Biwa, an ancient lake in Japan, and the role of the lake in the diversification of freshwater fish in western Japan, we established a molecular phylogenetic framework with an absolute time scale and inferred the historical demography of a large set of fish species in and around the lake. We used mtDNA sequences obtained from a total of 190 specimens, including 11 endemic species of Lake Biwa and their related species, for phylogenetic analyses with divergence time estimations and from a total of 2319 specimens of 42 species (including 14 endemics) occurring in the lake for population genetic analyses. Phylogenetic analysis suggested that some of the endemic species diverged from their closest relatives earlier (1.3–13.0 Ma) than the period in which the present environmental characteristics of the lake started to develop (ca. 0.4 Ma), whereas others diverged more recently (after 0.4 Ma). In contrast, historical demographic parameters suggested that almost all species, including endemic and nonendemic ones, expanded their populations after the development of the present lake environment. In phylogeographic analyses, common or very close haplotypes of some species were obtained from Lake Biwa and other regions of western Japan. The phylogenetic and historical demographic evidence suggests that there was a time lag between phylogenetic divergence and population establishment and that phenotypic adaptation of some endemic species to the limnetic environment occurred much later than the divergences of those endemic lineages. Population structure and phylogeographic patterns suggest that Lake Biwa has functioned not only as the center of adaptive evolution but also as a reservoir for fish diversity in western Japan.

Phylogeography of a salmonid fish, masu salmon Oncorhynchus masou subspecies‐complex, with disjunct distributions across the temperate northern Pacific

“…The co‐distributed salmonid fish, white‐spotted charr Salvelinus leucomaenis , is also characterised by having mtDNA haplotypes diagnostic from other populations (Kikko et al, ; Yamamoto, Morita, Kitano, et al, ). The present environment of Lake Biwa started to form c. 0.4 Ma (Tabata et al, and references therein). It has been inferred that the origin of O. masou subsp.…”

“…It has been inferred that the origin of O. masou subsp. diverged from the other subspecies c. 0.52 Ma (Tabata et al, ). All things considered, O. masou subsp., by its use of Lake Biwa, could have diverged from a common ancestor of masu salmon before large‐scale population expansion of the species occurred.…”

“…We used nucleotide substitution rates of 1.16% per million year for cytochrome‐ b region and 0.99% for ND‐5 region, which were obtained from the Bayesian phylogenetic analysis for O. masou subsp. (Tabata et al, ). The effective population size for the posterior distribution of the estimated parameter values was determined using Bayesian skyline plot analysis with the stepwise (constant) model, using TRACER ver.…”

“…Oncorhynchus masou subsp. is endemic to Lake Biwa, on central Honshu Island, an ancient lake with an origin dating back to at least c. 0.4 Ma (Tabata, Kakioka, Tominaga, Tomiya, & Watanabe, and references therein). Oncorhynchus masou subsp.…”

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

“…Lake Biwa is the oldest and largest lake in Japan formed approximately 4 Ma (Kawabe, , ; Yokoyama, ). According to Tabata, Kakioka, Tominaga, Komiya, and Watanabe (), Paleo‐Lake Biwa consisted of a series of lakes and marsh environments that existed from 4 to 0.4 Ma. After the Pliocene, the topographical and limnological features of Paleo‐Lake Biwa and Lake Tokai, located east of Paleo‐Lake Biwa successively changed: the paleo‐lake experienced: (a) Shallow and large stages (Lake Ohyamada >3.2 Ma; Lake Ayama 3.0–2.7 Ma); (b) A deep and large stage (Lake Koka 2.7–2.5 Ma), similar to the northern basin of the present Lake Biwa; (c) A second shallow and large stage (Lake Gamo 2.5–1.8 Ma); (d) A swamp‐like stage (1.8–1.0 Ma); and (e) A final shallow and large stage (Lake Katata 1.0–0.5 Ma) (Kawabe, , ).…”