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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.

SUBMITTER: Tabata R

PROVIDER: S-EPMC4798153 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:BackgroundCarp gudgeons (genus Hypseleotris) are a prominent part of the Australian freshwater fish fauna, with species distributed around the western, northern, and eastern reaches of the continent. We infer a calibrated phylogeny of the genus based on nuclear ultraconserved element (UCE) sequences and using Bayesian estimation of divergence times, and use this phylogeny to investigate geographic patterns of diversification with GeoSSE. The southeastern species have hybridized to form hemiclonal lineages, and we also resolve relationships of hemiclones and compare their phylogenetic placement in the UCE phylogeny with a hypothesis based on complete mitochondrial genomes. We then use phased SNPs extracted from the UCE sequences for population structure analysis among the southeastern species and hemiclones.ResultsHypseleotris cyprinoides, a widespread euryhaline species known from throughout the Indo-Pacific, is resolved outside the remainder of the species. Two Australian radiations comprise the bulk of Hypseleotris, one primarily in the northwestern coastal rivers and a second inhabiting the southeastern region including the Murray-Darling, Bulloo-Bancannia and Lake Eyre basins, plus coastal rivers east of the Great Dividing Range. Our phylogenetic results reveal cytonuclear discordance between the UCE and mitochondrial hypotheses, place hemiclone hybrids among their parental taxa, and indicate that the genus Kimberleyeleotris is nested within the northwestern Hypseleotris radiation along with three undescribed species. We infer a crown age for Hypseleotris of 17.3 Ma, date the radiation of Australian species at roughly 10.1 Ma, and recover the crown ages of the northwestern (excluding H. compressa) and southeastern radiations at 5.9 and 7.2 Ma, respectively. Range-dependent diversification analyses using GeoSSE indicate that speciation and extinction rates have been steady between the northwestern and southeastern Australian radiations and between smaller radiations of species in the Kimberley region and the Arnhem Plateau. Analysis of phased SNPs confirms inheritance patterns and reveals high levels of heterozygosity among the hemiclones.ConclusionsThe northwestern species have restricted ranges and likely speciated in allopatry, while the southeastern species are known from much larger areas, consistent with peripatric speciation or allopatric speciation followed by secondary contact. Species in the northwestern Kimberley region differ in shape from those in the southeast, with the Kimberley species notably more elongate and slender than the stocky southeastern species, likely due to the different topographies and flow regimes of the rivers they inhabit.

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Project description:BackgroundUnderstanding the causes of disparities in species diversity across taxonomic groups and regions is a fundamental aim in evolutionary biology. Addressing these questions is difficult because of the need for densely sampled phylogenies and suitable empirical systems.Methodology/principal findingsHere we investigate the cichlid fish radiation of Lake Tanganyika and show that per lineage diversification rates have been more than six times slower than in the species flocks of Lakes Victoria and Malawi. The result holds even at peak periods of diversification in Lake Tanganyika, ruling out the age of the lake as an explanation for slow average rates, and is robust to uncertainties over the calibration of cichlid radiations in geological time. Moreover, Lake Tanganyika lineages, irrespective of different biological characteristics (e.g. sexually dichromatic versus sexually monochromatic clades), have diversified at similar rates, falling within typical estimates across a range of plant and animal clades. For example, the mostly sexually dichromatic haplochromines, which have speciated explosively in Lakes Victoria and Malawi, have displayed modest rates in Lake Tanganyika (where they are called Tropheini).Conclusion/significanceOur results show that either the Lake Tanganyika environment is less conducive for cichlid speciation or the remarkable diversifying abilities of the haplochromines were inhibited by the prior occupancy of older radiations. Although the results indicate a dominant role for the environment in shaping cichlid diversification, differences in the timing of diversification among the Tanganyikan tribes indicate that biological differences were still important for the dynamics of species build-up in the lake. While we cannot resolve the timing of the radiation relative to the origin of the lake, because of the lack of robust geological date calibrations for cichlids, our results are consistent with a scenario that the different clades reflect independent adaptive radiations into different broad niches in the lake.

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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.

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