Fine scale genetic population structure of the freshwater and Omono types of nine‐spined stickleback Pungitius pungitius (L.) within the Omono River system, Japan

Abstract

The fine scale geographic population structure of two types of nine-spined stickleback Pungitius pungitius (the widely distributed freshwater type and a local endemic, the Omono type) within the Omono River system, Japan, was investigated. A principal components analysis of allele frequencies and neighbour-joining tree for pair-wise F ST values, based on 10 allozyme loci, revealed that the Omono type was comprised of four regional groups with relatively high genetic divergence. This grouping was also supported by hierarchical analysis of molecular variance (AMOVA) with a higher variance component among the regional groups, and by an exact test with significant genotypic differentiation for all sample pairs among the regional groups. Moreover, in the clustering of individuals using the Bayesian method, most of individuals in each regional group were assigned the corresponding cluster. On the other hand, there were less pronounced regional groups of the freshwater type, although AMOVA, exact test for genotypic differentiation and Bayesian analysis indicated genetic divergence between two sampling sites in lower reach of the Omono River and other sites. The results suggest that the Omono type represented an earlier colonization, with subsequent invasion of the freshwater type.

A phylogenomic perspective on diversity, hybridization and evolutionary affinities in the stickleback genusPungitius

“…In particular, an increasing amount of evidence for a high prevalence of admixture and hybridization has been transforming our view on how species evolve, and at the same time has made it clear that well-resolved phylogenies should not be taken for granted (e.g., Mallet et al, 2016). In this perspective, the well-resolved and robust phylogeny of the Pungitius species complex obtained in this study with a large number of nuclear genetic markers is noteworthy, especially given that there is evidence for weakly developed post-zygotic isolation and hybridization in this genus (Kobayashi, 1959;Tsuruta & Goto, 2006;Ziuganov & Gomeluk, 1985). Moreover, our discovery of four putative mitochondrial capture events testifies to past hybridization events, yet evidence for substantial introgression in nuclear genomes was not recovered in any of the species.…”

“…As none of the diverse populations of P. kaibarae from South Korea and Russia show mitonuclear incongruence (Bae & Suk, ; Takahashi et al, ), it appears that mitochondrial introgression occurred specifically in the Japanese P. kaibarae population after it split from these populations. It is also noteworthy that hybridization occurs between the Omono‐ and freshwater‐types in their areas of sympatry (Tsuruta & Goto, ). An alternative explanation for the mitonuclear incongruence is that the mitogenome carried by all extant P. pungitius populations was derived from P. sinensis , possibly in a hybridization event that occurred before the ancestors of the current P. pungitius populations colonized Europe and North America.…”

“…Third, current understanding of phylogenetic relationships in the Pungitius species complex resides heavily on mitochondrial DNA sequences (e.g., Bae & Suk, 2015;Takahashi & Goto, 2001;Teacher, Shikano, Karjalainen, & Merilä, 2011;Wang et al, 2015), and only a few studies-all based on either limited geographical or taxon sampling-have utilized nuclear genetic information (Aldenhoven, Miller, Corneli, & Shapiro, 2010;Bae & Suk, 2015;Haglund et al, 1992;Natri, Merilä, & Shikano, 2019;Shikano, Ramadevi, Shimada, & Merilä, 2010;Takahashi et al, 2016;Takata, Goto, & Yamazaki, 1987b;Wang, Shikano, Persat, & Merilä, 2017). Phylogenetic studies based on a large number of nuclear loci are motivated by the well-known limitations of phylogenetic and phylogeographical inferences based on mitochondrial information (e.g., Ballard & Whitlock, 2004;Hey & Machado, 2003;Toews & Brelsford, 2012), as well as by the evidence for weak post-zygotic isolation (Kobayashi, 1959;Takahashi, Nagai, & Goto, 2005;Tsuruta & Goto, 2006;Ziuganov & Gomeluk, 1985), and hybridization in this genus (Denys et al, 2018;Niwa, 1987;Takahashi et al, 2016;Takahashi & Takata, 2000;Wang et al, 2017;Natri et al, 2019).…”

Nine‐spined stickleback (Pungitius pungitius): an emerging model for evolutionary biology research

“…Recent phylogeographic and population genetic studies have clarified the evolutionary history of nine‐spined sticklebacks in Europe, North America, and Japan . In Europe, the species is divided into two distinct evolutionary lineages (Western and Eastern) that were formed during the Pleistocene glaciations .…”

Comparative Analysis of Japanese Three-Spined Stickleback Clades Reveals the Pacific Ocean Lineage Has Adapted to Freshwater Environments while the Japan Sea Has Not

“…Nonetheless the nine-spined stickleback ( Pungitius spp. ) could also act as a competitor, having adapted to freshwater environments connected to the Sea of Japan [80] , [81] . Nine-spined stickleback are also absent from the Pacific coast, except in Hokkaido potentially allowing greater ecological opportunity for the Pacific Ocean lineage although this has not been explicitly studied.…”