Marine Biology

, 164:106 | Cite as

Phylogeography of the yellowfin goby Acanthogobius flavimanus in native and non-native distributions

  • Shotaro Hirase
  • Sherrie Chambers
  • Kathryn Hassell
  • Melissa Carew
  • Vincent Pettigrove
  • Kiyoshi Soyano
  • Masaki Nagae
  • Wataru Iwasaki
Original paper

Abstract

Species introductions have been recognized as one of the principal threats to marine environments worldwide. Comparison of genetic data between native and non-native populations can provide key information, such as origin and population demography during the colonization process, which assists in understanding the mechanisms of invasion success in marine environments. The yellowfin goby, Acanthogobius flavimanus, is a large goby native to northeastern Asia, typically inhabiting muddy bottoms of bays, estuaries, and rivers, and is considered a pest where it has invaded coastal areas of the United States and Australia. Here, we analyzed mitochondrial DNA control region sequences of several yellowfin goby populations from both native and non-native distributions. The phylogenetic tree showed no intra-specific lineages, which is in contrast with previous phylogeographic studies that have shown deep genetic divergence in other coastal marine gobies around the Japanese archipelago. On the other hand, at the population level, we found significant genetic differentiation between northern and southern groups in the native distribution, which may be attributed to a rapid population expansion event of the southern group. Our analyses suggest that the origin of the northern California population is Tokyo Bay, but we were unable to identify the original source populations of the southern California and Melbourne populations. These populations showed greatly differing genetic diversities, suggesting their different demographic histories. This study contributes a new perspective on the genetic diversity of multiple populations of the yellowfin goby, as well as representing an example of the relationships between genetic diversity and invasion success.

Supplementary material

227_2017_3137_MOESM1_ESM.eps (996 kb)
Supplementary Fig. 1. Median-joining network of the 137 haplotypes of the yellowfin goby. Each line between the haplotypes indicates a single nucleotide substitution. Small black circles between haplotypes represent intermediate hypothesized haplotypes. Circle sizes reflect the sum of the haplotype frequencies of all locations (EPS 995 kb)

References

  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 et al (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 427:7–18CrossRefGoogle Scholar
  3. Amsellem L, Noyer J, Le Bourgeois T et al (2000) Comparison of genetic diversity of the invasive weed Rubus alceifolius Poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:443–455CrossRefGoogle Scholar
  4. Baltz DM (1991) Introduced fishes in marine systems and inland seas. Biol Conserv 56:151–177CrossRefGoogle Scholar
  5. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefGoogle Scholar
  6. Barrett S, Richardson B (1986) Genetic attributes of invading species. In: Groves RH, Burdon JJ (eds) Ecology of biological invasions. Cambridge University Press, Cambridge, pp 21–33Google Scholar
  7. Bell JD, Steffe AS, Talbot RB (1987) The oriental goby, Acanthogobius flavimanus, colonizes a third estuary in New South Wales, Australia. Ichthyol Res 34:227–230Google Scholar
  8. Blaxter J (1986) Development of sense organs and behaviour of teleost larvae with special reference to feeding and predator avoidance. Trans Am Fish Soc 115:98–114CrossRefGoogle Scholar
  9. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefGoogle Scholar
  10. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154CrossRefGoogle Scholar
  11. Bradman H, Grewe P, Appleton B (2011) Direct comparison of mitochondrial markers for the analysis of swordfish population structure. Fish Res 109:95–99CrossRefGoogle Scholar
  12. Bray DJ, Gomon MF (2011) Fishes. In: Taxonomic Toolkit for marine life of Port Phillip Bay, Museum Victoria. http://portphillipmarinelife.net.au
  13. Brittan MR, Albrecht AB, Hopkirk JB (1963) An oriental goby collected in the San Joaquin River delta near Stockton, California. Calif Fish Game 49:302–304Google Scholar
  14. Brittan MR, Hopkirk JD, Conners JD et al (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
  15. Brogan MW (1994) Distribution and retention of larval fishes near reefs in the Gulf of California. Mar Ecol Prog Ser 115:1–13CrossRefGoogle Scholar
  16. Brown JE, Stepien CA (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Mol Ecol 18:64–79Google Scholar
  17. Burton RS (1983) Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar Biol Lett 4:193–206Google Scholar
  18. Dawson M, Louie K, Barlow M et al (2002) Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California Transition Zone. Mol Ecol 11:1065–1075CrossRefGoogle Scholar
  19. Dlugosch K, Parker I (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefGoogle Scholar
  20. Donaldson KA, Wilson RR Jr (1999) Amphi-panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 13:208–213CrossRefGoogle Scholar
  21. 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
  22. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  23. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefGoogle Scholar
  24. 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 131:479–491Google Scholar
  25. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  26. Felsenstein J (1993) Phylogeny inference package (PHYLIP). Version 3.5. University of Washington, SeattleGoogle Scholar
  27. Frankham R, Lees K, Montgomery ME et al (1999) Do population size bottlenecks reduce evolutionary potential? Anim Conserv 2:255–260CrossRefGoogle Scholar
  28. Haaker PL (1979) Two Asiatic gobiid fishes, Tridentiger trigonocephalus and Acanthogobius flavimanus, in southern California. Bull South Calif Acad Sci 78:56–61Google Scholar
  29. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefGoogle Scholar
  30. 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
  31. Hirase S, Ikeda M, Kanno M et al (2012) Phylogeography of the intertidal goby Chaenogobius annularis associated with paleoenvironmental changes around the Japanese Archipelago. Mar Ecol Prog Ser 450:167–179CrossRefGoogle Scholar
  32. Hirase S, Takeshima H, Nishida M et al (2016) Parallel mitogenome sequencing alleviates random rooting effect in phylogeography. Genome Biol Evol 8:1267–1278CrossRefGoogle Scholar
  33. Hoarau G, Coyer J, Veldsink J et al (2007) Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol Ecol 16:3606–3616CrossRefGoogle Scholar
  34. Hoese D (1973) The introduction of the gobiid fishes Acanthogobius flavimanus and Tridentiger trigonocephalus into Australia. Koolewong 2:3–5Google Scholar
  35. Itaki T, Ikehara K, Motoyama I et al (2004) Abrupt ventilation changes in the Japan Sea over the last 30 ky: evidence from deep-dwelling radiolarians. Palaeogeogr Palaeoclimatol Palaeoecol 208:263–278CrossRefGoogle Scholar
  36. Japanese Association of Zoos and Aquariums (2007) Propagation commendation in fiscal year 2006. J Jpn Assoc Zoos Aquar 48:70 (Japan)Google Scholar
  37. Japanese Association of Zoos and Aquariums (2008) Propagation commendation in fiscal year 2007. J Jpn Assoc Zoos Aquar 49:64–65 (Japan)Google Scholar
  38. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13CrossRefGoogle Scholar
  39. Kang M, Buckley YM, Lowe AJ (2007) Testing the role of genetic factors across multiple independent invasions of the shrub Scotch broom (Cytisus scoparius). Mol Ecol 16:4662–4673CrossRefGoogle Scholar
  40. Kanou K, Sano M, Kohno H (2005) Ontogenetic diet shift, feeding rhythm, and daily ration of juvenile yellowfin goby Acanthogobius flavimanus on a tidal mudflat in the Tama River estuary, central Japan. Ichthyol Res 52:319–324CrossRefGoogle Scholar
  41. Katayama S, Sakai K, Iwata T et al (2000) Life history of Japanese common goby Acanthogobius flavimanus in Hiroura Lagoon of Natori River mouth. Bull Miyagi Pref Fish Res Dev Center 16:93–97 (Japan)Google Scholar
  42. Kojima S, Hayashi I, Kim D et al (2004) Phylogeography of an intertidal direct-developing gastropod Batillaria cumingi around the Japanese Islands. Mar Ecol Prog Ser 276:161–172CrossRefGoogle Scholar
  43. 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 20:143–164CrossRefGoogle Scholar
  44. Lisiecki LE, Raymo ME (2005) A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20:PA1003Google Scholar
  45. Meng L, Moyle PB, Herbold B (1994) Changes in abundance and distribution of native and introduced fishes of Suisun Marsh. Trans Am Fish Soc 123:498–507CrossRefGoogle Scholar
  46. 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
  47. Molnar JL, Gamboa RL, Revenga C et al (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  48. Neilson ME, Wilson RR (2005) mtDNA singletons as evidence of a post-invasion genetic bottleneck in yellowfin goby Acanthogobius flavimanus from San Francisco Bay, California. Mar Ecol Prog Ser 296:197–208CrossRefGoogle Scholar
  49. Ni G, Li Q, Kong L et al (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Mol Ecol 23:534–548CrossRefGoogle Scholar
  50. Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20CrossRefGoogle Scholar
  51. Prentis PJ, Wilson JR, Dormontt EE et al (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294CrossRefGoogle Scholar
  52. Provan J, Wattier RA, Maggs CA (2005) Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Mol Ecol 14:793–803CrossRefGoogle Scholar
  53. Rambaut A, Drummond A (2009) Tracer version 1.5. 0. WWW document. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 1 Sept 2016
  54. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  55. Rius M, Turon X, Bernardi G et al (2015) Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biol Invasions 17:869–885CrossRefGoogle Scholar
  56. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  57. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228Google Scholar
  58. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  59. Sakai K, Katayama S, Iwata T (2000) Life history of the Japanese common goby, Acanthogobius flavimanus in the Matsushima Bay. Bull Miyagi Pref Fish Res Dev Center 16:85–92 (Japan)Google Scholar
  60. Shimizu M (1984) Fishes and shellfishes in Tokyo Bay (1). Aquabiology 30:9–13 (Japan)Google Scholar
  61. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  62. 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 364:277–289 (Japan) Google Scholar
  63. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  64. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+ C-content biases. Mol Biol Evol 9:678–687Google Scholar
  65. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  66. Tringali MD, Bert TM, Seyoum S et al (1999) Molecular phylogenetics and ecological diversification of the transisthmian fish genus Centropomus (Perciformes: Centropomidae). Mol Phylogenet Evol 13:193–207CrossRefGoogle Scholar
  67. Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968CrossRefGoogle Scholar
  68. Vlaming VL (1972) Environmental control of teleost reproductive cycles: a brief review. J Fish Biol 4:131–140CrossRefGoogle Scholar
  69. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513Google Scholar
  70. Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728CrossRefGoogle Scholar
  71. Xia X, Xie Z, Salemi M et al (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Shotaro Hirase
    • 1
    • 2
    • 3
  • Sherrie Chambers
    • 4
  • Kathryn Hassell
    • 4
  • Melissa Carew
    • 4
  • Vincent Pettigrove
    • 4
  • Kiyoshi Soyano
    • 5
  • Masaki Nagae
    • 6
  • Wataru Iwasaki
    • 2
    • 3
    • 7
  1. 1.Fisheries Laboratory, Graduate School of Agricultural and Life SciencesThe University of TokyoHamamatsuJapan
  2. 2.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoBunkyo-ku, TokyoJapan
  3. 3.Atmosphere and Ocean Research InstituteThe University of TokyoKashiwaJapan
  4. 4.Centre for Aquatic Pollution Identification and Management (CAPIM), Biosciences 4University of MelbourneParkvilleAustralia
  5. 5.Institute for East China Sea Research, Organization for Marine Science and TechnologyNagasaki UniversityNagasakiJapan
  6. 6.Faculty of Environmental ScienceNagasaki UniversityNagasakiJapan
  7. 7.Department of Computational Biology and Medical Sciences, Graduate School of Frontier SciencesThe University of TokyoKashiwaJapan

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