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. 2016 Mar 16;6(8):2601-23.
doi: 10.1002/ece3.2070. eCollection 2016 Apr.

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

Ryoichi Tabata  1 , Ryo Kakioka  2 , Koji Tominaga  3 , Takefumi Komiya  1 , Katsutoshi Watanabe  1
Affiliations

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

Ryoichi Tabata et al. Ecol Evol. .

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.

Keywords: Ancient lake; Lake Biwa; cytochrome b; divergence time; historical demography; mtDNA.

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Figures

Figure 1
Figure 1
Endemic and semiendemic fishes in Lake Biwa. Note that a semiendemic species is not endemic to Lake Biwa, but its distribution is mostly restricted to Lake Biwa.
Figure 2
Figure 2
Sampling localities of specimens used for phylogenetic and population genetic analyses. For locality codes, see Tables S1 and S2.
Figure 3
Figure 3
Bayesian phylogenetic trees of each fish group including species/subspecies endemic to Lake Biwa based on mtDNA 16S rRNA, CO1, ND5, cyt b, and CR gene sequences. Outgroups are not shown. The trees were dated by the random local clock model with node age constraints (C1–C6; see Table 2 and Fig. S1). All nodes are supported by a Bayesian posterior probability of 1.0, except for those denoted by numbers. Horizontal bars at nodes show credible intervals as 95% highest posterior density. For codes of nodes (a–o), see Table 3. For results including outgroups, see Fig. S1.
Figure 4
Figure 4
(A) Distribution of uncorrected P distances and (B) timing of divergence between endemic fishes and their relatives in Lake Biwa. a, Oncorhynchus masou subsp. “Lake Biwa trout” (Salmonidae); b, Carassius cuvieri (Cyprinidae); c, Gnathopogon caerulescens (Cyprinidae); d, Sarcocheilichthys biwaensis and S. variegatus microoculus (Cyprinidae); e, Squalidus biwae biwae (Cyprinidae); f, Opsariichthys uncirostris (Cyprinidae); g, Silurus lithophilus (Siluridae; vs. one sister cryptic clade of S. asotus); h, S. lithophilus (Siluridae; vs. all clades of S. asotus); i, Silurus biwaensis (Siluridae); j, Gymnogobius isaza (Gobiidae); k, Cottus reinii (lacustrine type) (Cottoidae).
Figure 5
Figure 5
(A) Mismatch distributions and statistical parsimony networks of mtDNA cytochrome b haplotypes of fishes in Lake Biwa. In mismatch distribution results, the bars of the histogram represent the frequencies of the observed pairwise differences. The solid lines represent the expected distributions under a sudden expansion model. In haplotype networks, the sizes of the circles are proportional to the numbers of individuals. A square indicates a missing haplotype. The number of missing haplotypes (≥2) is indicated in the squares. The branches indicate one substitution. (B) The typical results of Bayesian skyline plots for representative endemic species. The central bold line represents the median value for the relative effective population size, and the solid area denotes the 95% upper and lower credible limits. For detailed statistics and results of other species, see Table 4 and Table S6 and Fig. S2.
Figure 6
Figure 6
Timing of population expansion in the populations of endemic and nonendemic fishes in Lake Biwa. The squares represent the time based on the mismatch distribution analysis. The circles represent the time estimated with the Bayesian skyline plot analysis. Bars denote the 95% upper and lower credible limits.
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