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Quaternary-related genetic differentiation and parallel population dynamics of the Eurasian Jay (Garrulus glandarius) in the circum-Japan Sea region

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Abstract

The circum-Japan Sea region (CJSR) greatly impacted animal diversity in the Eastern Palearctic during the Quaternary. However, its role in avian diversification has been underestimated because of the high dispersal capabilities of birds over the sea. We investigated the phylogeographic and demographic history of the Eurasian Jay (Garrulus glandarius), focusing on CJSR populations. We sequenced a total of 1744 bp of mitochondrial DNA (cytochrome b and control region) from 73 samples. Together with the database sequences, we reconstructed a phylogenetic tree for the Eurasian Jay over the Palearctic. The earliest phylogenetic divergence was inferred to be related to geological vicariance between the Japanese archipelago and Eurasian mainland around the Pliocene–Pleistocene boundary. Several demographic analyses have suggested that there are two divergent subspecies across the CJSR, G. g. brandtii on the mainland, Sakhalin, and Hokkaido and G. g. japonicus in the archipelago. These simultaneously experienced population contractions to independent refugia and subsequent expansions around the last glacial period, i.e., parallel population dynamics. We suggest that the two landmasses of the CJSR were important for generating and preserving the phylogenetic structure of the Eurasian Jay.

Zusammenfassung

Quartäre genetische Differenzierung und parallele Populationsdynamik des Eichelhähers Garrulus glandarius in der Region um das Japanische Meer Die Region um das Japanische Meer (engl: Circum-Japan Sea Region; CJSR) hatte während des Quartärs einen starken Einfluss auf die Vielfalt der Tiere in der östlichen Paläarktis. Aufgrund der hohen Ausbreitungsfähigkeit der Vögel über das Meer wurde ihre Bedeutung für die ornithologische Diversität allerdings unterschätzt. Wir untersuchten die phylogeografische und demografische Geschichte des Eichelhähers Garrulus glandarius, wobei wir uns auf die CJSR-Populationen konzentrierten. Wir nahmen eine Neusequenzierung von insgesamt 1744 bp mitochondrialer DNA (Cytochrom b und Kontrollregion) aus 73 Proben vor. Zusammen mit Sequenzen aus Datenbanken rekonstruierten wir einen phylogenetischen Stammbaum für den Eichelhäher in der Paläarktis. Die früheste phylogenetische Aufspaltung stand demnach in Relation zu geologischen Vikarianzereignissen zwischen dem japanischen Archipel und dem eurasischen Festland, etwa zur Pliozän-Pleistozän-Grenze. Verschiedene demografische Analysen lassen vermuten, dass es in der CJSR zwei getrennte Unterarten gibt: G. g. brandtii auf dem Festland, auf Sachalin und Hokkaido sowie G. g. japonicus auf dem Archipel, deren Populationen sich gleichzeitig in individuelle Refugien zurückgezogen und in der Folge etwa zur Zeit der letzten Glazialperiode wieder ausgebreitet haben, also eine parallele Populationsdynamik zeigen. Wir nehmen an, dass die beiden Landmassen der CJSR eine wichtige Rolle bei der Entstehung und Aufrechterhaltung der populationsgenetischen Struktur des Eichelhähers innehatten.

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Acknowledgements

We are grateful to Kimiyuki Tsuchiya, Ya Red’kinm, S. Elsukov, A. Antonov, the Conservation Genome Resource Bank (CGRB) for Korean Wildlife, and the Center for Molecular Biodiversity Research, National Museum of Nature and Science, Tokyo for providing samples. For the earlier use of unpublished database sequences, we appreciate the generosity of Kyoko Iwami and Masaoki Takagi. We thank Shota Murakami for assistance with field sampling and laboratory experiments, and Yusuke Nishida for stimulating discussion.

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Correspondence to Daisuke Aoki.

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Conflicts of interest

This study was partly conducted with the support of a grant-in-aid for Scientific Research (C) to HS (no. 15K07177) from the Japan Society for the Promotion of Science (JSPS). The authors declare that they have no conflicts of interest.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed. This article does not involve any studies with human participants performed by any of the authors.

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Communicated by M. Wink.

Electronic supplementary material

Online Resource 1 List of the 34 subspecies of the Eurasian Jay with their distributions, subspecies group assignment, and shared morphological characteristics among subspecies in each subspecies group.

Online Resource 2 List of specimens and sequences from GenBank used in this study. The CR sequences were all ca. 600 bp, while complete coding sequences were used for Cytb, unless stated otherwise. Subspecies were assigned for each taxon of Eurasian Jay on the basis of the subspecies or the phylogroups to which they belong in this and previous studies (Akimova et al. 2007). Accession numbers denoted “this study” in the reference column were obtained from submissions to the DDBJ international DNA database

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Aoki, D., Kinoshita, G., Kryukov, A.P. et al. Quaternary-related genetic differentiation and parallel population dynamics of the Eurasian Jay (Garrulus glandarius) in the circum-Japan Sea region. J Ornithol 159, 1087–1097 (2018). https://doi.org/10.1007/s10336-018-1573-9

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  • DOI: https://doi.org/10.1007/s10336-018-1573-9

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