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Complex phylogeographic patterns in the intertidal goby Chaenogobius annularis around Kyushu Island as a boundary zone of three different seas

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Abstract

Paleoenvironmental changes in marginal seas on the coast of the northwestern Pacific during the Quaternary have caused genetic differentiation and subsequent secondary contacts between populations of coastal organisms in this region. However, little is known about how geographical isolation and the subsequent connection events associated with these multiple marginal seas have shaped the population structure of coastal organisms in the boundary area. The coastal area of Kyushu Island of the Japanese Archipelago, where the East China Sea (ECS), the Sea of Japan (SJ), and the Pacific Ocean (PO) adjoin within a narrow region, would be a suitable field for elucidating the effect of multiple vicariances. Herein, we conducted phylogeographical analyses of the intertidal goby Chaenogobius annularis, focusing on populations around Kyushu Island, using partial mitochondrial (mt) DNA sequences and analysis of 8 microsatellite (ms) DNA loci. We discovered a new lineage distributed along the coast of the ECS distinct from the already-known SJ and PO lineages, which we termed the ECS lineage. This ECS lineage showed remarkable mito-nuclear discordance: mtDNA analyses indicated that the ECS lineage is a highly diverged lineage branched from the PO lineage, whereas msDNA analyses suggested that the ECS lineage is closely related to the SJ lineage. This discordance could have been due to ancient hybridization. In addition, we detected SJ-PO and ECS-SJ hybrid zones on the western Seto Inland Sea and on the northwestern coast of Kyushu, respectively. Such a complex population structure suggests that the secondary contacts after multiple isolation events among marginal seas around Kyushu have a great impact on coastal biodiversity in the area and emphasize the peculiarities of the region.

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References

  • Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D (2013). Hybridization and speciation. J Evol Biol 26: 229–246

    Article  CAS  PubMed  Google Scholar 

  • Akihito, Akishinonomiya F, Ikeda Y, Aizawa M, Makino T, Umehara Y, Kai Y, Nishimoto Y, Hasegawa M, Nakabo T, Gojobori T (2008) Evolution of Pacific Ocean and the Sea of Japan populations of the gobiid species, Pterogobius elapoides and Pterogobius zonoleucus, based on molecular and morphological analyses. Gene 427:7–18

    Article  CAS  PubMed  Google Scholar 

  • Akihito, Iwata A, Kobayashi T, Ikeo K, Imanishi T, Ono H, Umehara Y, Hmamatsu C, Sugiyama K, Ikeda Y, Sakamoto K, Akishinonomiya F, Ohno S, Gojobori T (2000) Evolutionary aspects of gobioid fishes based upon a phylogenetic analysis of mitochondrial cytochrome b genes. Gene 259:5–15

    Article  CAS  PubMed  Google Scholar 

  • Akihito, Sakamoto K, Ikeda Y, Aizawa M (2013) Gobioidei. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 3rd edition. Tokai University Press, Hadano, pp 1347–1608, 2109–2211 (in Japanese)

  • Allio R, Donega S, Galtier N, Nabholz B (2017) Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Mol Biol Evol, 34: 2762–2772

    Article  CAS  PubMed  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160: 1217–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arlyza IS, Shen KN, Durand JD, Borsa P (2013) Mitochondrial haplotypes indicate parapatric-like phylogeographic structure in blue-spotted maskray (Neotrygon kuhlii) from the Coral Triangle region. J Hered 104: 725–733

    Article  CAS  PubMed  Google Scholar 

  • Bernatchez L, Glémet H, Wilson CC, Danzmann RG (1995) Introgression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 52:179–185

    Article  CAS  Google Scholar 

  • Carpenter KE, Barber PH, Crandall ED, Carmen A, Ablan-Lagman M, Ambariyanto, Mahardika GN, Manjaji-Matsumoto BM, Juinio-Meñez MA, Santos MD, Starger CJ, Toha AHA (2011). Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol 2011: 1–14

    Article  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16: 551–558

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620

    CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (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

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86: 485–486

    Article  Google Scholar 

  • Grant WS (2015) Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. J Hered 106: 333–346

    Article  PubMed  Google Scholar 

  • Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MHY, Hansen HF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Ž, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, De La Rasilla Marco, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S (2010) A draft sequence of the Neandertal genome. Science 328: 710–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirase S, Ikeda M (2014a) Divergence of mitochondrial DNA lineage of the rocky intertidal goby Chaenogobius gulosus around the Japanese Archipelago: reference to multiple Pleistocene isolation events in the Sea of Japan. Mar Biol 161:565–574

    Article  CAS  Google Scholar 

  • Hirase S, Ikeda M (2014b) Long-term vicariance and post-glacial expansion in the Japanese rocky intertidal goby Chaenogobius annularis. Mar Ecol Prog Ser 499:217–231

    Article  Google Scholar 

  • Hirase S, Ikeda M (2015) Hybrid population of highly divergent groups of the intertidal goby Chaenogobius annularis. J Exp Mar Biol Ecol 473:121–128

    Article  Google Scholar 

  • Hirase S, Ikeda M, Kanno M, Kijima A. (2012a) Phylogeography of the intertidal goby Chaenogobius annularis associated with paleoenvironmental changes around the Japanese Archipelago. Mar Ecol Prog Ser 450:167–179

    Article  CAS  Google Scholar 

  • Hirase S, Kanno M, Ikeda M, Kijima A (2012b) Evidence of the restricted gene flow within a small spatial scale in the Japanese common intertidal goby Chaenogobius annularis. Mar Ecol 33:481–489

    Article  Google Scholar 

  • Hirase S, Kokita T, Nagano AJ, Kikuchi K (2020) Genomic and phenotypic consequences of two independent secondary contact zones between allopatric lineages of the anadromous ice goby Leucopsarion petersii. Heredity 124: 223–235

    Article  CAS  PubMed  Google Scholar 

  • Hirase S, Takeshima H, Nishida M, Iwasaki W (2016) Parallel mitogenome sequencing alleviates random rooting effect in phylogeography. Genome Biol Evol, 8:1267–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 94

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamata H, Kodama K (1999) Volcanic history and tectonics of the Southwest Japan Arc. Isl Arc 8: 393–403

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kitamura A, Takano O, Takata H, Omote H (2001) Late Pliocene-early Pleistocene paleoceanographic evolution of Sea of Japan. Palaeogeogr Palaeoclimatol Palaeoecol 172:81–98.

    Article  Google Scholar 

  • Kodama K, Tashiro H, Takeuchi T (1995) Quaternary counterclockwise rotation of south Kyushu, southwest Japan. Geology 23: 823–826

    Article  Google Scholar 

  • Kobayashi H, Haino Y, Iwasaki T, Tezuka A, Nagano AJ, Shimada S (2018) ddRAD-seq based phylogeographic study of Sargassum thunbergii (Phaeophyceae, Heterokonta) around Japanese coast. Mar Environmen Res, 140: 104–113

    Article  CAS  Google Scholar 

  • Kokita T, Nohara K (2011) Phylogeography and historical demography of the anadromous fish Leucopsarion petersii in relation to geological history and oceanography around the Japanese Archipelago. Mol Ecol 20:143–164

    Article  PubMed  Google Scholar 

  • Kojima S, Segawa R, Hayashi I (1997) Genetic differentiation among populations of the Japanese turban shell Turbo (Batillus) cornutus corresponding to warm currents. Mar Ecol Prog Ser 150:149–155

    Article  Google Scholar 

  • Kojima S, Hayashi I, Kim D, Iijima A, Furota T (2004) Phylogeography of an intertidal direct-develo** gastropod Batillaria cumingi around the Japanese Islands. Mar Ecol Progr Ser 276:161–172

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206

    Article  CAS  PubMed  Google Scholar 

  • Leigh JW, Bryant D (2015) popart: full-feature software for haplotype network construction. Methods Ecol Evol 6: 1110–1116

    Article  Google Scholar 

  • Li GX, Li P, Liu Y, Qiao LL, Ma YY, Xu JS, Yang Z (2014) Sedimentary system response to the global sea level change in the East China Seas since the last glacial maximum. Earth-Sci Rev 139:390–405

    Article  Google Scholar 

  • Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol Ecol 16:275–288

    Article  CAS  PubMed  Google Scholar 

  • Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC (2005). Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14, 2459–2464

    Article  CAS  PubMed  Google Scholar 

  • McGuire JA, Linkem CW, Koo MS, Hutchison DW, Lappin AK, Orange DI, Lemos-Espinal J, Riddle BR, Jaeger JR (2007) Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards. Evolution 61: 2879–2897

    Article  CAS  PubMed  Google Scholar 

  • Murase A, Miki R, Motomura H (2017) Southern limits of distribution of the intertidal gobies Chaenogobius annularis and C. gulosus support the existence of a biogeographic boundary in southern Japan (Teleostei, Perciformes, Gobiidae). Zookeys (725):79–95

    Article  Google Scholar 

  • Nakano T, Sasaki T, Kase T (2010) Color polymorphism and historical biogeography in the Japanese patellogastropod limpet Cellana nigrolineata (Reeve) (Patellogastropoda: Nacellidae). Zool Sci 27: 811–820

    Article  Google Scholar 

  • Nei M, Kumar S (2000). Molecular evolution and phylogenetics. New York, Oxford University Press

    Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19: 153–170

    Article  CAS  PubMed  Google Scholar 

  • Ni G, Li Q, Kong LF, Yu H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Mol Ecol 23:534–548

    Article  PubMed  Google Scholar 

  • Ôki K (2002) Changes in depositional environments during the pot-glacial stage in Kagoshima Bay and seas around the Northern part of the Ryukyu Islands. The Quaternary Research (Daiyonki-Kenkyuu), 41:237–251 (in Japanese with English abstract)

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28: 2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86: 248–249

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223–225

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9: 552–569

    CAS  PubMed  Google Scholar 

  • Rohfritsch A, Borsa P (2005) Genetic structure of Indian scad mackerel Decapterus russelli: Pleistocene vicariance and secondary contact in the Central Indo-West Pacific Seas. Heredity 95: 315–326

    Article  CAS  PubMed  Google Scholar 

  • Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22: 939–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset F (2008). GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8: 103–106

    Article  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34: 3299–3302

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425

    CAS  PubMed  Google Scholar 

  • Sasaki T, Hattori J (1969) Comparative ecology of two closely related sympatric gobiid fishes living in tide pools. Jpn J Ichthyol 15:143–155 (in Japanese with English abstract)

    Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Sibuet JC, Letouzey J, Barbier F, Charvet J, Foucher JP, Hilde TW, Kimura M, Chiao LY, Marsset B, Muller C, Stéphan JF (1987) Back arc extension in the Okinawa Trough. J Geophys Res Sol Ea 92: 14041–14063

    Article  Google Scholar 

  • Sloan DB, Havird JC, Sharbrough J (2017) The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol Ecol 26: 2212–2236

    Article  PubMed  PubMed Central  Google Scholar 

  • Takezaki N, Nei M, Tamura K (2010) POPTREE2: Software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Mol Biol Evol 27: 747–752

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaki K, Honza E (1991) Global tectonics and formation of marginal basins: role of the western Pacific. Episodes 14: 224–230

    Article  Google Scholar 

  • Tanaka K (2009) Ariake Bay-indigenous fishes: A present from the continent in glacial age. In: Nature Conservation Committee of Ichthyological Society of Japan (ed) Fishes in estuarine and tidal flat ecosystems: status of endangered fishes in Ariake Sound. Tokai University Press, Hadano, pp 107–122 (in Japanese)

  • Taylor DJ, Hebert PD (1993) Cryptic intercontinental hybridization in Daphnia (Crustacea): the ghost of introductions past. Proc R Soc Lond B Biol Sci 254: 163–168

    Article  Google Scholar 

  • Teske PR, Sandoval-Castillo J, Golla TR, Emami-Khoyi A, Tine M, von der Heyden S, Beheregaray LB (2019) Thermal selection as a driver of marine ecological speciation. Proceedings of the Royal Society B 286: 2018–2023

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang PX (1999) Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar Geol 156:5–39

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370

    CAS  PubMed  Google Scholar 

  • Wilson CC, Bernatchez L (1998) The ghost of hybrids past: fixation of arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush). Mol Ecol 7: 127–132

    Article  Google Scholar 

  • Xu J, Chan TY, Tsang LM, Chu KH (2009) Phylogeography of the mitten crab Eriocheir sensu stricto in East Asia: pleistocene isolation, population expansion and secondary contact. Mol Phylogenetics Evol 52:45–56

    Article  CAS  Google Scholar 

  • Yamanaka T, Miyabe S, Sawai Y, Shimoyama S (2010) Geochemical and diatom evidence of transition from freshwater to marine environments in the Aira Caldera and Kagoshima Bay, Japan, during post-glacial sea-level rise. J Asian Earth Sci 39: 386–395

    Article  Google Scholar 

  • Yashima K (1994) A geomorphological study of the caldrons in the Seto Inland Sea. Rep Hydrogr Res, 30:237–327 (in Japanese with English abstract)

    Google Scholar 

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Acknowledgement

We would like to express great gratitude to the members of the laboratory for their helpful advice. We are grateful to Daisuke Kanemaru, Graduate School of Sciences, The University of Tokyo for his assistance in literature collection. This work was supported by the Japan Society for the Promotion of Science (KAKENHI 18H02493).

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Kato, S., Arakaki, S., Kikuchi, K. et al. Complex phylogeographic patterns in the intertidal goby Chaenogobius annularis around Kyushu Island as a boundary zone of three different seas. Ichthyol Res 68, 86–100 (2021). https://doi.org/10.1007/s10228-020-00772-4

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