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.
Similar content being viewed by others
References
Akimova A, Haring E, Kryukov S, Kryukov A (2007) First insights into a DNA sequence based phylogeny of the Eurasian Jay Garrulus glandarius. Russ J Ornithol 16:567–575
Bazarova VB, Klimin MA, Mokhova LM, Orlova LA (2008) New pollen records of Late Pleistocene and Holocene changes of environment and climate in the Lower Amur River basin, NE Eurasia. Quat Int 179:9–19. https://doi.org/10.1016/j.quaint.2007.08.015
Bouckaert R, Heled J, Kühnert D et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1003537
Chen D, Zhang X, Kang H et al (2012) Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and mainland-migrated island populations. PLoS One. https://doi.org/10.1371/journal.pone.0047268
Chung C-H, Lim HS, Il Yoon H (2006) Vegetation and climate changes during the Late Pleistocene to Holocene inferred from pollen record in Jinju area, South Korea. Geosci J 10:423–431. https://doi.org/10.1016/j.quaint.2010.06.002
Chung C-H, Lim HS, Lee HJ (2010) Vegetation and climate history during the late Pleistocene and early Holocene inferred from pollen record in Gwangju area, South Korea. Quat Int 227:61–67. https://doi.org/10.1016/j.quaint.2010.06.002
Cramp S (1994) Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic. Crows to Finches, vol VIII. Oxford University Press, New York
de Kort SR, Clayton NS (2006) An evolutionary perspective on caching by corvids. Proc R Soc B 273:417–423. https://doi.org/10.1098/rspb.2005.3350
del Hoyo J, Collar NJ (2014) HBW and bird life international illustrated checklist of the birds of the world. volume 1: Non-passerines. Lynx Edicions, Barcelona
del Hoyo J, Collar NJ (2016) HBW and bird life international illustrated checklist of the birds of the world, vol 2: passerines. Lynx Edicions, Barcelona
Dickinson EC, Christidis L (eds) (2014) The Howard and Moore complete checklist of the birds of the world, 4th ed, vol 2. Aves, Eastbourne
Dobson M, Kawamura Y (1998) Origin of the Japanese Mammal Fauna: allocation of extant species to historically-based categories. Quat Res 37:385–395. https://doi.org/10.4116/jaqua.37.385
dos Anjos L (2009) Eurasian Jay (Garrulus glandarius). In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the birds of the world, vol 14. Bush-shrikes to old world sparrows. Lynx Edicions, Barcelona, pp 558–589
Drovetski SV, Zink RM, Fadeev IV et al (2004) Mitochondrial phylogeny of Locustella and related genera. J Avian Biol 35:105–110. https://doi.org/10.1111/j.0908-8857.2004.03217.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Filatov DA (2009) Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25:3189–3190. https://doi.org/10.1093/bioinformatics/btp572
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gallagher S, Kitamura A, Iryu Y et al (2015) The Pliocene to recent history of the Kuroshio and Tsushima currents: a multi-proxy approach. Prog Earth Planet Sci 2:17. https://doi.org/10.1186/s40645-015-0045-6
Gill F, Donsker D (2018) IOC world bird list (v8.1). http://www.worldbirdnames.org/. Accessed 27 Mar 2018
Goodwin D (1986) Crows of the world, 2nd edn. British Museum (Natural History), London
Hanazaki K, Tomozawa M, Suzuki Y et al (2017) Estimation of evolutionary rates of mitochondrial DNA in two Japanese wood mouse species based on calibrations with quaternary environmental changes. Zool Sci 34:201–210. https://doi.org/10.2108/zs160169
Haring E, Gamauf A, Kryukov A (2007) Phylogeographic patterns in widespread corvid birds. Mol Phylogenet Evol 45:840–862. https://doi.org/10.1016/j.ympev.2007.06.016
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Harrison SP, Yu G, Takahara H, Prentice IC (2001) Paleovegetation (communications arising): diversity of temperate plants in east Asia. Nature 413:129–130. https://doi.org/10.1038/35093166
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694
Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 8:289. https://doi.org/10.1186/1471-2148-8-289
Hewitt GM (1996) Some genetic consequences of ice ages, and their role, in divergence and speciation. Biol J Linn Soc 58:247–276. https://doi.org/10.1006/bijl.1996.0035
Hikida T (2003) Biogeography of reptiles in islands in East Asia—geographic distribution from views of molecular and morphological studies. Seibutsu Kagaku 54:205–220
Hirata D, Abramov AV, Baryshnikov GF, Masuda R (2014) Mitochondrial DNA haplogrouping of the brown bear, Ursus arctos (Carnivora: Ursidae) in Asia, based on a newly developed APLP analysis. Biol J Linn Soc 111:627–635. https://doi.org/10.1111/bij.12219
Ho SYW, Lanfear R, Bromham L et al (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101. https://doi.org/10.1111/j.1365-294X.2011.05178.x
Holt BG, Lessard J-P, Borregaard MK et al (2013) An update of Wallace’s zoogeographic regions of the world. Science 339:74–78. https://doi.org/10.1126/science.1228282
Hope AG, Waltari E, Dokuchaev NE et al (2010) High-latitude diversification within Eurasian least shrews and Alaska tiny shrews (Soricidae). J Mammal 91:1041–1057. https://doi.org/10.1644/09-MAMM-A-402.1
Igarashi Y (2016) Vegetation and climate during the LGM and the last deglaciation on Hokkaido and Sakhalin Islands in the northwest Pacific. Quat Int 425:28–37. https://doi.org/10.1016/j.quaint.2016.05.018
Igarashi Y, Oba T (2006) Fluctuations in the East Asian monsoon over the last 144 ka in the northwest Pacific based on a high-resolution pollen analysis of IMAGES core MD01-2421. Quat Sci Rev 25:1447–1459. https://doi.org/10.1016/j.quascirev.2005.11.011
Igarashi Y, Iwahana G, Sento N et al (2003) Surface pollen data from different vegetation types in northeastern Russia. Quat Res 42:413–425. https://doi.org/10.4116/jaqua.42.413
Iwasaki T, Aoki K, Seo A, Murakami N (2012) Comparative phylogeography of four component species of deciduous broad-leaved forests in Japan based on chloroplast DNA variation. J Plant Res 125:207–221. https://doi.org/10.1007/s10265-011-0428-8
Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298. https://doi.org/10.1093/bib/bbn013
Katoh K, Kuma KI, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518. https://doi.org/10.1093/nar/gki198
Kayvanfar N, Aliabadian M, Niu X et al (2017) Phylogeography of the Common Pheasant Phasianus colchicus. Ibis 159:430–442. https://doi.org/10.1111/ibi.12455
Kinoshita G, Nunome M, Han S-H et al (2012) Ancient colonization and within-island vicariance revealed by mitochondrial DNA phylogeography of the mountain hare (Lepus timidus) in Hokkaido, Japan. Zool Sci 29:776–785. https://doi.org/10.2108/zsj.29.776
Kinoshita G, Sato JJ, Meschersky IG et al (2015) Colonization history of the sable Martes zibellina (Mammalia, Carnivora) on the marginal peninsula and islands of northeastern Eurasia. J Mammal 96:172–184. https://doi.org/10.1093/jmammal/gyu021
Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima current into the sea of Japan between 3.5 and 0.8 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 236:355–366. https://doi.org/10.1016/j.palaeo.2005.11.015
Kryukov A, Spiridonova L, Nakamura S et al (2012) Comparative phylogeography of two crow species: jungle crow Corvus macrorhynchos and carrion crow Corvus corone. Zool Sci 29:484–492. https://doi.org/10.2108/zsj.29.484
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li W-H (1977) Distribution of nucleotide differences between two randomly chosen cistrons in a population of variable size. Genetics 85:331–337. https://doi.org/10.1016/0040-5809(77)90003-X
Li X, Dong F, Lei F et al (2016) Shaped by uneven Pleistocene climate: mitochondrial phylogeographic pattern and population history of white wagtail Motacilla alba (Aves: Passeriformes). J Avian Biol 47:263–274. https://doi.org/10.1111/jav.00826
Mckay BD (2012) A new timeframe for the diversification of Japan’s mammals. J Biogeogr 39:1134–1143. https://doi.org/10.1111/j.1365-2699.2011.02666.x
Mokhova L, Tarasov P, Bazarova V, Klimin M (2009) Quantitative biome reconstruction using modern and late quaternary pollen data from the southern part of the Russian far east. Quat Sci Rev 28:2913–2926. https://doi.org/10.1016/j.quascirev.2009.07.018
Morioka H, Sakane T (1980) Subalpine Avifauna of the Ohmine Moutain Range in the Kii Peninsula, Japan. Mem Natl Sci Museum 13:53–58
Nishiumi I, Kim C-H (2015) Assessing the potential for reverse colonization among Japanese birds by mining DNA barcode data. J Ornithol 156:325–331. https://doi.org/10.1007/s10336-015-1247-9
Nishiumi I, Yao C-T, Saito DS, Lin R-S (2006) Influence of the last two glacial periods and the late Pliocene on the latitudinal population structure of resident songbirds in the Far East. Mem Natl Sci Museum 44:11–20
Norman JA, Rheindt FE, Rowe DL, Christidis L (2007) Speciation dynamics in the Australo-Papuan Meliphaga honeyeaters. Mol Phylogenet Evol 42:80–91. https://doi.org/10.1016/j.ympev.2006.05.032
Okaura T, Quang ND, Ubukata M, Harada K (2007) Phylogeographic structure and late quaternary population history of the Japanese oak Quercus mongolica var. crispula and related species revealed by chloroplast DNA variation. Genes Genet Syst 82:465–477. https://doi.org/10.1266/ggs.82.465
Oshida T, Abramov A, Yanagawa H, Masuda R (2005) Phylogeography of the Russian flying squirrel (Pteromys volans): implication of refugia theory in arboreal small mammal of Eurasia. Mol Ecol 14:1191–1196. https://doi.org/10.1111/j.1365-294X.2005.02475.x
Päckert M, Sun YH, Strutzenberger P et al (2015) Phylogenetic relationships of endemic bunting species (Aves, Passeriformes, Emberizidae, Emberiza koslowi) from the eastern Qinghai-Tibet Plateau. Vertebr Zool 65:135–150
R Core Team (2016) R: A language and environment for statistical computing. https://www.r-project.org. Accessed 2 November 2011
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer. http://tree.bio.ed.ac.uk/software/tracer. Accessed 2 November 2017
Razzhigaeva NG, Ganzei LA, Belyanina NI (2010) First data on landscape evolution in the southern Kurile Islands at the Pleistocene–Holocene transition. Dokl Earth Sci 430:57–61. https://doi.org/10.1134/S1028334X10010137
Řičánková VP, Robovský J, Riegert J (2014) Ecological structure of recent and last glacial mammalian faunas in northern Eurasia: the case of Altai-Sayan refugium. PLoS One 9:e85056. https://doi.org/10.1371/journal.pone.0085056
Rogers AR (1995) Genetic evidence for a pleistocene population explosion. Evolution 49:608–615
Saitoh T, Alström P, Nishiumi I et al (2010) Old divergences in a boreal bird supports long-term survival through the Ice Ages. BMC Evol Biol. https://doi.org/10.1186/1471-2148-10-35
Saitoh T, Sugita N, Someya S et al (2015) DNA barcoding reveals 24 distinct lineages as cryptic bird species candidates in and around the Japanese Archipelago. Mol Ecol Resour 15:177–186. https://doi.org/10.1111/1755-0998.12282
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, New York
Sato JJ (2017) A review of the process of mammalian faunal assembly in Japan: insights from molecular phylogenetics. In: Motokawa M, Kajihara H (eds) Species diversity of animals in Japan. Springer, Tokyo
Tada R (1994) Paleoceanographic evolution of the Japan Sea. Palaeogeogr Palaeoclimatol Palaeoecol 108:487–508. https://doi.org/10.1016/0031-0182(94)90248-8
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/molbev/msl149
Untergasser A, Nijveen H, Rao X et al (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:71–74. https://doi.org/10.1093/nar/gkm306
Waltari E, Cook JA (2005) Hares on ice: phylogeography and historical demographics of Lepus arcticus, L. othus, and L. timidus (Mammalia: Lagomorpha). Mol Ecol 14:3005–3016. https://doi.org/10.1111/j.1365-294X.2005.02625.x
Weir JT, Schluter D (2004) Ice sheets promote speciation in boreal birds. Proc R Soc Lond B 271:1881–1887. https://doi.org/10.1098/rspb.2004.2803
Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328. https://doi.org/10.1111/j.1365-294X.2008.03742.x
Weißensteiner M (2013) Morphological and genetical differences of two subspecies of the Masked Bunting Emberiza spodocephala in Far Eastern Russia. Karl-Franzens University of Graz
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Ethical standards
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.
Additional information
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
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-018-1573-9