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

Abstract

Climate oscillations during the Pleistocene had profound effects on the evolutionary history of freshwater fishes now distributed across northern temperate regions. The extent of continental glaciation on the western side of the North Pacific, including areas of East Asia, was more limited as compared with regions of North America, Europe and high-latitude areas of the North Pacific. Therefore, the effects of climate oscillations might have influenced species in dissimilar ways depending on the species' distribution. We used mitochondrial DNA (mtDNA) and microsatellite DNA (msDNA) markers to clarify the evolutionary history of masu salmon Oncorhynchus masou subspecies-complex (family Salmonidae) distributed in historically non-glaciated regions in the western North Pacific. No marked regional or subspecies-specific mtDNA haplotype associations were recognised, except for O. masou subsp., a lacustrine form endemic to Lake Biwa, an ancient lake in central Honshu. The landlocked subspecies O. masou formosanus, with a disjunct distribution on Taiwan Island, exhibited no diagnostic population features differing from the other subspecies, in either mtDNA or msDNA markers. Mismatch distribution and Bayesian skyline plot analyses indicated relatively recent range expansion and rapid population growth for masu salmon during the last glacial period (c. 0.1-0.15 Ma). Contrary to the mtDNA genealogy, Bayesian clustering using msDNA showed two main genetic clusters, mainly northern populations of the subspecies O. m. masou and populations of the subspecies O. m. ishikawae in southern areas of the Japanese Archipelago. Notably, O. m. formosanus on Taiwan Island was included in the O. m. masou group, and O. masou subsp. was included in the O. m. ishikawae group. Our results suggest that the masu salmon subspecies-complex in historically non-glaciated regions of the Temperate Northern Pacific is characterised by weak population structuring and shallow genetic differentiation among the subspecies, except for O. masou subsp. owing to its long isolation in Lake Biwa. Incomplete lineage sorting and historical inter-subspecies hybridisation, possibly due to secondary contact, seem to be plausible explanations for discrepancies in the mitochondrial DNA genealogy and nuclear DNA genetic structure.