Hidden mitochondrial DNA divergence in the Lake Biwa endemic goby Gymnogobius isaza: implications for its evolutionary history

Abstract

The gobiid Gymnogobius isaza is an endemic species that has adapted remarkably to the pelagic environment in Lake Biwa, Japan, a representative ancient lake in East Asia. To obtain clues that would reveal the origin and evolution of this species, we conducted phylogenetic and population genetic analyses based on partial sequences of the mitochondrial cytochrome b gene. Consistent with previous studies, our Bayesian phylogenetic analysis with a relaxed molecular clock model reconfirmed a sister relationship between G. isaza and Gymnogobius urotaenia + Gymnogobius petschiliensis, with a divergence time of about 2.9 million years (Myr), and provided an evolutionary rate of 3.0 %/Myr (pairwise) for their clade. Population genetic analysis revealed two distinct mtDNA groups in G. isaza, which were estimated to have diverged 0.66 million years ago (Mya) at the Lake Katata stage of Paleo-Lake Biwa, preceding the origin of the present Lake Biwa environment with its extensive deep pelagic area (0.3–0.4 Mya). A dumbbell-like haplotype network and bimodal mismatch distribution suggested that the population of G. isaza experienced secondary contact between two genetically differentiated populations. Demographic parameters from mismatch distribution analysis and Bayesian skyline plot analysis suggested that both of the mtDNA groups of G. isaza exhibited a signal of sudden population expansion at approximately the same time (80–90 thousand years ago) during the last glacial period after the development of the present Lake Biwa. These results imply the complex population history of G. isaza, including genetic isolation and secondary contact following differentiation from its relatives in the Pliocene.