Genetic isolation by distance in the yellowfin goby populations revealed by RAD sequencing

  • Shotaro HiraseEmail author
  • Ayumi Tezuka
  • Atsushi J. Nagano
  • Kiyoshi Kikuchi
  • Wataru Iwasaki
Full Paper


Population genetic studies of marine species sometimes find no clear patterns of genetic differentiation, but signals of geographic gene flow typified by isolation by distance (IBD) due to high dispersal ability. A previous study of mitochondrial DNA of the yellowfin goby Acanthogobius flavimanus indicated that this species also does not have clearly differentiated population groups around the Japanese archipelago, in contrast with other coastal goby species that have highly differentiated groups between the Sea of Japan and Pacific Ocean populations. Here, to clearly reveal phylogeographic structures of the yellowfin goby around the Japanese archipelago, we conducted large-scale RAD-sequencing analysis of their nuclear genomic SNP loci. As a result, IBD patterns were confirmed across the yellowfin goby populations, and the larval dispersal distance of this species was revealed to be approximately 19 km on average. In addition, different larval dispersal distances were estimated for its Sea of Japan and Pacific Ocean populations, suggesting that different coastal environments and/or ecological features may affect its dispersal rates. These results would provide foundations for ecological and conservation studies of the yellowfin goby and coastal fishes having similar dispersal strategy to this species.


RAD sequencing Acanthogobius flavimanus Isolation by distance Population structure 



The authors thank Kyushu and Tokushima prefecture lodges of Japan Sport Fishing Foundation, local fishing tackle stores in Japan (Jyoshu-Ya Miyagino store, Point Tokushima store, Anguru Koyaura store, Otaru-fishing PAPA, Kameya-Tsurigu Matsue store), and R. Tabata, S. Hayasaka, and T. Mikekado for providing specimens. This work was supported by the Ministry of Education, Culture, Sports, Science, and Technology (KAKENHI 221S0002 and Project “Construction of the platform for intellectual cooperation”) and the Japan Society for the Promotion of Science (KAKENHI 18H02493, 16H06154, and 26850131).


  1. Akihito, Sakamoto K, Ikeda Y, Sugiyama K (2002) Suborder Gobioidei. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, English edn. Tokai University Press, Tokyo, pp 1139–1310Google Scholar
  2. Akihito, Fumihito A, 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 427:7–18CrossRefPubMedGoogle Scholar
  3. Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12:246CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664CrossRefPubMedPubMedCentralGoogle Scholar
  5. Baltz DM (1991) Introduced fishes in marine systems and inland seas. Biol Conserv 56:151–177CrossRefGoogle Scholar
  6. Banks SC, Piggott MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064CrossRefPubMedGoogle Scholar
  7. Binks RM, Byrne M, McMahon K, Pitt G, Murray K, Evans RD (2019) Habitat discontinuities form strong barriers to gene flow among mangrove populations, despite the capacity for long-distance dispersal. Divers Distrib 25:298–309CrossRefGoogle Scholar
  8. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics:btu170Google Scholar
  9. Brittan MR, Albrecht AB, Hopkirk JB (1963) An oriental goby collected in the San Joaquin River delta near Stockton, California. Cal Fish and Game 49:302–304Google Scholar
  10. Brittan MR, Hopkirk JD, Conners JD, Martin M (1970) Explosive spread of the oriental goby Acanthogobius flavimanus in the San Francisco Bay-Delta region of California. Proc Calif Acad Sci 38:207–214Google Scholar
  11. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3-Genes Genom Genet 1:171–182Google Scholar
  12. Dotsu Y, Mito S (1955) On the breeding-habits, larvae and young of a goby, Acanthogobius flavimanus (Temminck et Schlegel). Jpn J Ichthyol 4:153–161Google Scholar
  13. Dotsu Y, Tsutsumi T (1959) The reproductive behaviour in the gobiid fish, Pterogobius elapoides (Günther). Rep Fac Fish Nagasaki Univ 8:186–190Google Scholar
  14. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  15. Green AL, Maypa AP, Almany GR, Rhodes KL, Weeks R, Abesamis RA, Gleason MG, Mumby PJ, White AT (2015) Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biol Rev 90:1215–1247CrossRefPubMedGoogle Scholar
  16. Haaker PL (1979) Two Asiatic gobiid fishes, Tridentiger trigonocephalus and Acanthogobius flavimanus, in southern California. Bull South Calif Acad Sci 78:56–61Google Scholar
  17. Hirase S, Chambers S, Hassell K, Carew M, Pettigrove V, Soyano K, Nagae M, Iwasaki W (2017) Phylogeography of the yellowfin goby Acanthogobius flavimanus in native and non-native distributions. Mar Biol 164:106CrossRefGoogle Scholar
  18. Hirase S, Ikeda M (2014) 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 161:565–574CrossRefGoogle Scholar
  19. Hirase S, Ikeda M, Kanno M, Kijima A (2012) Phylogeography of the intertidal goby Chaenogobius annularis associated with paleoenvironmental changes around the Japanese Archipelago. Mar Ecol Prog Ser 450:167–179CrossRefGoogle Scholar
  20. Hirase S, Kokita T, Nagano AJ, Kikuchi K (2019) Genomic and phenotypic consequences of two independent secondary contact zones between allopatric lineages of the anadromous ice goby Leucopsarion petersii. Heredity. CrossRefPubMedGoogle Scholar
  21. Hirase S, Takeshima H, Nishida M, Iwasaki W (2016) Parallel mitogenome sequencing alleviates random rooting effect in phylogeography. Genome Biol Evol 8:1267–1278CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kanou K (2004) Diet shift with settlement in the yellowfin goby Acanthogobius flavimanus at a tidal mudflat. La mer 41:67–72Google Scholar
  23. Kanou K, Sano M, Kohno H (2005) Larval and juvenile fishes occurring with flood tides on an intertidal mudflat in the Tama River estuary, central Japan. Ichthyol Res 52:158–164CrossRefGoogle Scholar
  24. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  25. Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, Absher DM, Grimwood J, Schmutz J, Myers RM et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461:1079–1083CrossRefPubMedPubMedCentralGoogle Scholar
  26. Koike F, Iwasaki K (2011) A simple range expansion model of multiple pathways: the case of nonindigenous green crab Carcinus aestuarii in Japanese waters. Biol Invasions 13:459–470CrossRefGoogle Scholar
  27. 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 20:143–164CrossRefPubMedGoogle Scholar
  28. Kokita T, Takahashi S, Kumada H (2013) Molecular signatures of lineage‐specific adaptive evolution in a unique sea basin: the example of an anadromous goby Leucopsarion petersii. Mol Ecol 22:1341–1355CrossRefPubMedGoogle Scholar
  29. Leaché AD, Banbury BL, Felsenstein J, De Oca AN-M, Stamatakis A (2015) Short tree, long tree, right tree, wrong tree: new acquisition bias corrections for inferring SNP phylogenies. Syst Biol 64:1032–1047CrossRefPubMedPubMedCentralGoogle Scholar
  30. Luu K, Bazin E, Blum MG (2017) pcadapt: an R package to perform genome scans for selection based on principal component analysis. Mol Ecol Resour 17:67–77CrossRefPubMedGoogle Scholar
  31. Matsui S, Inui R, Kai Y (2014) Annotated checklist of gobioid fishes (Perciformes, Gobioidei) from Wakasa Bay, Sea of Japan. Bull Osaka Mus Nat Hist 68:1–25Google Scholar
  32. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  33. Middleton M (1982) The oriental goby, Acanthogobius flavimanus (Temminck and Schlegel), an introduced fish in the coastal waters of New South Wales, Australia. J Fish Biol 21:513–523CrossRefGoogle Scholar
  34. Oba T, Kato M, Kitazato H, Koizumi I, Omura A, Sakai T, Takayama T (1991) Paleoenvironmental changes in the Japan Sea during the last 85,000 years. Paleoceanography 6:499–518CrossRefGoogle Scholar
  35. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  36. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7: e37135CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pinsky ML, Saenz-Agudelo P, Salles OC, Almany GR, Bode M, Berumen ML, Andréfouët S, Thorrold SR, Jones GP, Planes S (2017) Marine dispersal scales are congruent over evolutionary and ecological time. Curr Biol 27:149–154CrossRefPubMedGoogle Scholar
  38. Puebla O, Bermingham E, McMillan WO (2012) On the spatial scale of dispersal in coral reef fishes. Mol Ecol 21:5675–5688CrossRefPubMedGoogle Scholar
  39. Ravinet M, Takeuchi N, Kume M, Mori S, Kitano J. 2014. Comparative analysis of Japanese three-spined stickleback clades reveals the Pacific Ocean lineage has adapted to freshwater environments while the Japan Sea has not. PLoS One 9:24CrossRefGoogle Scholar
  40. Shimizu M (1984) Fishes and shellfishes in Tokyo Bay (1). Aquabiology 30: 9-13Google Scholar
  41. Sasaki T., Hattori J. (1969) Comparative ecology of two closely related sympatric gobiid fishes living in tide pools. Jap J Ichthyol 15:143–155.Google Scholar
  42. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  43. Stamatakis A (2006) Phylogenetic models of rate heterogeneity: a high performance computing perspective. Proceedings 20th IEEE International Parallel and Distributed Processing Symposium. IEEE, p 278Google Scholar
  44. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefPubMedGoogle Scholar
  45. Suzuki N, Sakurai N, Sugihara T (1989) Development of eggs, larvae and juveniles of the oriental goby Acanthogobius flavimanus reared in the laboratory. Suisan Zoshoku 364:277–289Google Scholar
  46. Teske PR, Golla TR, Sandoval-Castillo J, Emami-Khoyi A, van der Lingen CD, von der Heyden S, Chiazzari B, van Vuuren BJ, Beheregaray LB (2018) Mitochondrial DNA is unsuitable to test for isolation by distance. Sci Rep 8:8448CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tsutsumi T, Dotu Y (1961) The reproductive behavior in the gobiid fish, Pterogobius zonoleucus Jordan et Snyder. Bull Fac Fish Nagasaki Univ 10:149–155Google Scholar
  48. Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259CrossRefGoogle Scholar

Copyright information

© The Ichthyological Society of Japan 2019

Authors and Affiliations

  • Shotaro Hirase
    • 1
    • 2
    • 3
    Email author
  • Ayumi Tezuka
    • 4
  • Atsushi J. Nagano
    • 4
  • Kiyoshi Kikuchi
    • 1
  • Wataru Iwasaki
    • 2
    • 3
  1. 1.Fisheries Laboratory, Graduate School of Agricultural and Life SciencesUniversity of TokyoHamamatsuJapan
  2. 2.Department of Biological Sciences, Graduate School of ScienceUniversity of TokyoTokyoJapan
  3. 3.Atmosphere and Ocean Research InstituteUniversity of TokyoKashiwaJapan
  4. 4.Faculty of AgricultureRyukoku UniversityOtsuJapan

Personalised recommendations