Multiple colonizations of Lake Biwa by Sarcocheilichthys fishes and their population history

Abstract

Rapid adaptation and speciation have not been well documented for organisms in Lake Biwa, Japan, the oldest ancient lake in East Asia. To examine these processes, we focused on the divergence of Sarcocheilichthys gudgeons and conducted phylogeographic and population genetic analyses using mitochondrial DNA sequences and microsatellite data. No remarkable genetic differentiation was found between two species, S. biwaensis and S. variegatus microoculus, both endemic to Lake Biwa, whereas this species group, including S. v. variegatus, was genetically divided into three major regional groups: the Lake Biwa, Ise Bay, and western groups. Divergent mtDNA haplotypes were included within the Lake Biwa and western groups, strongly suggesting secondary contacts among allopatrically isolated populations. Dating for mtDNA phylogeny using a geological constraint suggested the colonization of Lake Biwa by multiple Sarcocheilichthys lineages that diverged from each other in the early-middle Pleistocene. Coalescent-based population analyses indicated that the local populations colonized the rocky bottom habitat in Lake Biwa from other habitats after the Last Glacial Maximum, likely reflecting past environmental changes in the lake, including the disappearance of rocky areas during the glacial climate. Divergent morphological adaptation in Sarcocheilichthys associated with substrate type may have rapidly proceeded along with environmental changes. Keywords Ancient lake • Central Japan • Gobioninae • Historical demography • Phylogeography • Trophic polymorphism (73%) haplotype (Fig. 2). A subclade of clade A, consisting of A15 and A16, and a tip haplotype, A18, were detected exclusively from the Chugoku region. Clade B haplotypes were obtained from the Lake Biwa, Kinki, and Chugoku regions, but showed some regional distribution patterns. The most interior haplotype of clade C (C03) was exclusively found in Kyushu, but the tip haplotypes were shared by specimens from the Lake Biwa, Kinki, and Chugoku regions. Clade D was endemic to the Yura River system (Kinki), and clade E was the earliest divergent group and was endemic to the Ise Bay area (Figs. 2, 3). Node tMRCA*(mean*±*SE) 95%*HPD

Genetic population structure of Hemigrammocypris rasborella (Cyprinidae) inferred from mtDNA sequences

“…Oryzias latipes is another exception in which the most divergent haplotype group is found from western Kyushu to the Ryukyu Islands (Takehana et al 2003), although the species shows some salinity tolerance. Rather, the largest divergence is found in the easternmost populations (Ise Bay area and the east) of some cyprinids (e.g., Biwia zezera, Watanabe et al 2010a;Sarcocheilichthys variegatus;Komiya et al 2013). The Ise Bay area harbors several endemic species and populations, including freshwater fishes (Watanabe 2012) and marsh plants (Ueda 1989).…”

“…For example, in some cyprinids widely occurring in the lowlands of western Japan, the easternmost populations around the Ise Bay area (Fig. 1) exhibit large divergence from other populations, as evidenced by mitochondrial DNA (mtDNA) data (Watanabe et al 2010a;Komiya et al 2013). This suggests that a mountain system (the Suzuka Mountains), which forms a geological barrier dividing watersheds, has had a notable impact on population structure and the regional heterogeneity of freshwater fauna.…”

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

“…f 44 specimens from Tominaga et al (2009Tominaga et al ( , 2015. g From Komiya et al (2011Komiya et al ( , 2014. h Three specimens from Harada et al (2002); 113 specimens from Tabata and Watanabe (2013).…”

“…; Komiya et al. ); hence, it has been inferred that they recently diverged or are in the process of differentiation. However, the phylogenetic origins and divergence times of most endemics of Lake Biwa have not been elucidated.…”

“…For example, representative endemic fishes, such as Gnathopogon caerulescens (a cyprinid, presumably adapted to the pelagic environment) and Gymnogobius isaza (a goby, presumably adapted to the deep pelagic area), were derived from their extant closest relatives much earlier (2.5-3.0 Ma) than the formation of the present environments (Harada et al 2002;Kakioka et al 2013;Tabata and Watanabe 2013). In contrast, other endemic cyprinids, such as Sarcocheilichthys biwaensis and Sarcocheilichthys variegatus microoculus, are, from a genetic perspective, scarcely differentiated from their sister species (Komiya et al 2011;Komiya et al 2014); hence, it has been inferred that they recently diverged or are in the process of differentiation. However, the phylogenetic origins and divergence times of most endemics of Lake Biwa have not been elucidated.…”