Contrasting life histories contribute to divergent patterns of genetic diversity and population connectivity in freshwater sculpin fishes

Abstract

BackgroundLife history characteristics are considered important factors influencing the evolutionary processes of natural populations, including the patterns of population genetic structure of a species. The sister species Cottus hangiongensis and C. koreanus are small bottom-dwelling freshwater sculpin fishes from South Korea that display marked life history divergence but are morphologically nearly indistinguishable. Cottus hangiongensis evolved an ‘amphidromous’ life history with a post-hatching pelagic larval phase. They spawn many small eggs in the low reaches of rivers, and hatched larvae migrate to the sea before returning to grow to maturity in the river mouth. In contrast, C. koreanus evolved a ‘fluvial’ landlocked type with benthic larvae. They release a smaller number of larger eggs, and the larvae undergo direct development, remaining benthic in the upstream rivers throughout their entire lives. We tested whether there were differences in patterns and levels of within-population genetic diversities and spatial population structure between the two closely related Korean sculpins using mitochondrial DNA control region sequences and seven nuclear microsatellite loci.ResultsThe combined analyses of both marker sets revealed that C. hangiongensis harboured considerably higher levels of within-population genetic diversities (e.g. haplotype/allelic richness, heterozygosities) than C. koreanus. In contrast, the fluvial sculpin exhibited noticeably more spatial population structure than did the amphidromous sculpin, as suggested by pairwise FST statistics. The finding that C. hangiongensis individuals comprised a single random mating population across the east-flowing river basins in the Korean Peninsula, whereas C. koreanus individuals comprised genetically discrete individual populations, was further supported by an individual-based Bayesian population assignment and also factorial correspondence analyses.ConclusionsThe higher genetic diversity, but lower population structure, of the amphidromous sculpin relative to the fluvial sculpin may have resulted from its greater larval dispersal and also possibly, higher fecundity accompanied by an amphidromous life history. Hence, we conclude that contrasting early life histories – including the presence or absence of the pelagic larval phase – may have led to divergent patterns of within-population genetic diversities and spatial population structure between the sister Cottus species following speciation from a common ancestor of marine sculpin.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1171-8) contains supplementary material, which is available to authorized users.

Environmental effects, gene flow and genetic drift: Unequal influences on genetic structure across landscapes

“…This interpopulation connection can lead to species‐specific patterns of spatial genetic structure, as found among the two species examined in our study. The different genetic responses can reflect differences in their biology in terms of factors intrinsic to the population and/or to the life‐history traits of the species (Baek et al, 2018; Nukazawa et al, 2017; Whiteley et al, 2004). Although SM is distributed across the whole watershed and HO could not colonize most of the upstream and downstream branches, the two species both have wide potential distributions based on our niche modelling (see Figure 2).…”

Genetic structure and diversity of amphidromous sculpin in Shiretoko, a mountainous peninsula in Japan

“…In the case of the genus Cottus (Teleostei: Cottidae), a highly diversified sculpin group that comprises more than 60 species worldwide (Goto et al 2015), although genetic diversity in species with fluvial life-history has been studied in relation to dams (Hänfling and Weetman 2006;Junker et al 2012) or environments (Ruppert et al 2017;Nakajima et al 2021), there are not many studies pertaining to species with diadromous life history. Additionally, a few studies treating genetic data of diadromous species have usually focused on macroevolutionary processes such as speciation, and have not assessed and discussed recent changes in genetic diversity (e.g., Tsukagoshi et al 2013;Dennenmoser et al 2014Dennenmoser et al , 2017Kanno et al 2018; but see Baek et al 2018), even though benthic fish are particularly susceptible to river-crossing structures (Terui and Miyazaki 2017). Considering that diadromous fish usually exhibit high mobility and connectivity between neighboring tributaries, it will be necessary to identify the group of strongly connected populations (subpopulation structure) and to evaluate the genetic diversity of each subpopulation unit.…”

“…Cottus hangiongensis is a diadromous benthic fish that is distributed along the Sea of Japan in Russia, Korea, and northern Japan (Baek et al 2018). In Japan, this species is distributed on the Sea of Japan side from Central Honshu to Hokkaido Island, with a discontinuous distribution on the Sea of Okhotsk side of Hokkaido and around the Tsugaru Strait (Goto 1981).…”

“…From the perspective of conservation, although studies have been conducted on what kind of environment should be improved to increase suitable habitat (Goto 1981;Kitagawa et al 2021), research on conservation genetics is scarce. The only population genetic study of C. hangiongensis using microsatellite loci was conducted by Baek et al (2018), who evaluated the genetic structure and diversity of this species on the east coast of Korea and revealed the absence of genetic structure and highly maintained genetic diversity. However, since this is an example of one region with a relative abundance of rivers where fish can run up, we may not be able to generalize this pattern.…”

Tracking climate change in the spatial distribution pattern and the phylogeographic structure of Hyrcanian wood frog,Rana pseudodalmatina(Anura: Ranidae)

“…populations, with species-specific life histories and demographics also contributing to shaping species distributions and their temporal dynamics (Baek et al, 2018;Bell et al, 2010;Hua, 2013;Safner et al, 2011;Schierenbeck, 2017). Numerous phylogeographic studies have shown that during cold phases of the last glacial period the distribution ranges of many species contracted to climatic refugia (Bao et al, 2015;Leipold et al, 2017;Malekoutian et al, 2020;Song et al, 2018).…”