Ice age land bridges to continental islands: Repeated migration of the forest‐dwelling sable in northeastern Asia

Author:

Kinoshita Gohta1ORCID,Sato Takuma23ORCID,Murakami Shota4ORCID,Monakhov Vladimir5ORCID,Kryukov Alexey P.6,Frisman Lyubov V.7,Tsunamoto Yoshihiro8,Suyama Yoshihisa8,Murakami Takahiro9,Suzuki Hitoshi10,Sato Jun J.11ORCID

Affiliation:

1. Ecological Genetics Laboratory National Institute of Genetics Mishima Shizuoka Japan

2. The Institute of Regional Studies Okinawa University Naha Japan

3. Hokkaido Regional Environment Office, Ministry of the Environment Sapporo Japan

4. Department of General Systems Studies, Graduate School of Arts and Sciences The University of Tokyo Tokyo Japan

5. Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences (IPAE UB RAS) Yekaterinburg Russia

6. Laboratory of Evolutionary Zoology and Genetics, Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch Russian Academy of Sciences Vladivostok Russia

7. Institute for Complex Analysis of Regional Problems, Far East Branch Russian Academy of Sciences Birobidzhan Russia

8. Field Science Center, Graduate School of Agricultural Science Tohoku University Osaki Miyagi Japan

9. Shiretoko Museum Shari Hokkaido Japan

10. Course in Ecological Genetics, Graduate School of Environmental Science Hokkaido University Sapporo Hokkaido Japan

11. Laboratory of Zoology, Department of Biotechnology Fukuyama University Fukuyama Hiroshima Japan

Abstract

AbstractAimThe continental island system comprising Sakhalin, Hokkaido and the southern Kuril Islands (SHSK) in northeastern Asia serves as one of the southernmost habitats for many boreal and arctic organisms, with colonization via land bridges formed during glacial periods. To understand the impacts of past land‐bridge formation under Quaternary climate changes across SHSK, we investigated the demographic history of forest‐dwelling marten species.LocationSakhalin, Hokkaido and the southern Kuril Islands in northeastern Asia.TaxonSable, Martes zibellina (Carnivora, Mustelidae).MethodsWe employed multiplexed inter‐simple sequence repeat genotyping by sequencing (MIG‐seq) to obtain genome‐wide single nucleotide polymorphisms (SNPs). We tested possible scenarios of colonization and diversification for SHSK sables using several population genetics approaches including clustering analysis, population tree estimation and approximate Bayesian computation modelling. We also examined haplotype diversity for the mitochondrial ND2 gene.ResultsThe genetic diversity of the island populations and their affinity for continental populations were found to be higher in the order Sakhalin > Hokkaido > Iturup in both nuclear SNP and mitochondrial DNA analyses. Demographic analyses indicated that the sable migrated repeatedly from the continent, particularly to the neighbouring Sakhalin Island. However, only an earlier colonized lineage has persisted on marginal Iturup Island since the Middle Pleistocene. The stronger effects of repeated migrations and/or isolation influenced by the distance to the continent have shaped the contemporary genetic diversity and differentiation of sable populations in SHSK.Main ConclusionsGenome‐wide and comprehensive sampling approaches demonstrated that the forest‐dwelling sable had long‐term persistence with partial admixture of multiple lineages in SHSK, suggesting the existence of forest corridors and refugia on the islands during the last several glacial periods. The SHSK system of continental islands is valuable for understanding the impacts of Quaternary climate changes on the genetic diversity and evolutionary histories of boreal organisms.

Funder

Japan Society for the Promotion of Science

Publisher

Wiley

Subject

Ecology,Ecology, Evolution, Behavior and Systematics

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