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Phylogeography of the Chinese false gudgeon, Abbottina rivularis, in East Asia, with special reference to the origin and artificial disturbance of Japanese populations

  • Nian-Hong Jang-LiawEmail author
  • Koji Tominaga
  • Chungung Zhang
  • Yahui Zhao
  • Jun Nakajima
  • Norio Onikura
  • Katsutoshi WatanabeEmail author
Full Paper

Abstract

The Chinese false gudgeon, Abbottina rivularis, is a common cyprinid fish that is widely distributed throughout continental East Asia, but exhibits a restricted, discontinuous distribution in western Japan, including Honshu and Kyushu islands. In this study, analyses of mitochondrial (cytochrome b) and nuclear (glyt, myh6, and RAG1) genes were conducted to investigate patterns and magnitudes of intraspecific differentiation among A. rivularis populations in Japan and adjacent continental areas. Phylogenetic analysis of the mitochondrial gene sequences resolved four major lineages—the Japan lineage (JL), a northern continental lineage (NCL), and two southern continental lineages (SCL1 and SCL2)—with uncorrected pairwise sequence distances of 9.4–15.2% (estimated divergence times, 7.9–17.1 Myr). Two lineages (JL and SCL1) occurred in both the Honshu and Kyushu districts of Japan. Compared with populations in continental areas, most Japanese populations exhibited less genetic diversity. The JL was divided into two well-differentiated sub-lineages distributed on Honshu and Kyushu islands, respectively. Kyushu Island, as well as areas on Honshu where the species is known to have been introduced, also harbored the SCL1 lineage, which constituted most of the populations on Kyushu. The applied nuclear DNA data strongly suggest that hybridization between the Japan and continental lineages has occurred on Kyushu Island. The artificial introduction hypothesis, instead of a two-origin scenario, best explains the origin of the SCL1 in Japan.

Keywords

Abbottina rivularis Freshwater fish Phylogeography East Asia Artificial introduction Mitochondrial DNA (mtDNA) Nuclear DNA 

Notes

Acknowledgements

We would like to express our sincerest appreciation to A. Goto, S.-R. Jeon, S. Mori, T. Mukai, H. Sakai, and C. S. Tzeng for their generous donation of tissue samples; and to T. Abe and H. Egi for their kind help with fieldwork. We are also grateful to I. Koizumi and two anonymous reviewers for their helpful comments and suggestions on the manuscript. This study was supported in part by JSPS KAKENHI (nos. 18570086, 19405011, 21370035, 26291079, 26250044, and 17H03720) and the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of Kyoto University.

Supplementary material

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Supplementary material 1 (DOCX 12 kb)
10228_2019_686_MOESM2_ESM.docx (17 kb)
Supplementary material 2 (DOCX 16 kb)
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Supplementary material 3 (DOCX 12 kb)

References

  1. Aoyagi H (1957) General notes on the freshwater fishes of the Japanese Archipelago. Taishukan, TokyoGoogle Scholar
  2. Aoyama S, Watanabe S, Ishikawa S, Nishida M, Tsukamoto K (1999) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161CrossRefGoogle Scholar
  3. Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New YorkCrossRefGoogle Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Bǎnǎrescu PM, Nalbant TT (1973) Pisces, Teleostei. Cyprinidae (Gobioninae). Das Tierreich 93:1–304Google Scholar
  6. Beheregary LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol Ecol 17:3754–3774Google Scholar
  7. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10: e1003537CrossRefGoogle Scholar
  8. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633CrossRefGoogle Scholar
  9. Chan KMA, Levin SA (2005) Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 59:720–729CrossRefGoogle Scholar
  10. Chu XL, Chen YR (1989) The fishes of Yunnan, China. Part I. Cyprinidae. Science Press, BeijingGoogle Scholar
  11. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  12. Doadrio I, Domìnguez O (2004) Phylogenetic relationships within the fish family Goodeidae based on cytochrome b sequence data. Mol Phylogenet Evol 31:416–430CrossRefGoogle Scholar
  13. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88.  https://doi.org/10.1371/journal.pbio.0040088 CrossRefGoogle Scholar
  14. 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 10:564–567CrossRefGoogle Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  16. Hashiguchi Y, Kado T, Kimura S, Tachida H (2006) Comparative phylogeography of two bitterlings, Tanakia lanceolata and T. limbata (Teleostei, Cyprinidae), in Kyushu and adjacent districts of western Japan, based on mitochondrial DNA analysis. Zool Sci 23:309–322CrossRefGoogle Scholar
  17. Hayashi K, Kim EJ, Onikura N (2013) Growth and habitat use of the Chinese false gudgeon, Abbottina rivularis, in and irrigation channel near the Ushizu River, northern Kyushu Island, Japan. Ichthyol Res 60:218–226CrossRefGoogle Scholar
  18. He H, Li YH, Cao K, Li MY, Fu CZ (2017) Taxonomy and phylogenetic relationships of the genus Abbottina fishes in the subfamily Gobioninae. Acta Hydrobiologica Sinica 41:843–852Google Scholar
  19. Horikawa M, Nakajima J, Mukai T (2007) Distribution of indigenous and non-indigenous mtDNA haplotypes of Biwia zezera (Cyprinidae) in northern Kyushu, Japan. Jpn J Ichthyol 54:149–159Google Scholar
  20. Hosoya K (2001) Abbottina rivularis. In: Kawanabe H, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan. Yama-Kei Publish, TokyoGoogle Scholar
  21. Hosoya K (2002) Leptobotia curta. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, English edn. Tokai University Press, TokyoGoogle Scholar
  22. Hsieh CF (2002) Composition, endemism and phytogeographical affinities of the Taiwan flora. Taiwania 47:298–310Google Scholar
  23. Kawahara R, Miya M, Mabuchi K, Near TJ, Nishida M (2009) Stickleback phylogenies resolved: Evidence from mitochondrial genomes and 11 nuclear genes. Mol Phylogenet Evol 50:401–404CrossRefGoogle Scholar
  24. Kim J-M, Kennett J P (1998) Paleoenvironmental changes associated with the Holocene marine transgression, Yellow Sea (Hwanghae). Mar Micropaleontol 34:71–89CrossRefGoogle Scholar
  25. Kimizuka Y, Kobayasi H (1983) Geographic distributions of karyological races of Cobitis biwae (Cobitididae). Jpn J Ichthyol 30:308–312Google Scholar
  26. Kimura T (1985) Nihon-retto, III. The Japanese Archipelago. Kokin-shoin, TokyoGoogle Scholar
  27. Kita Y, Kato M (2004). Molecular phylogeny of Cladopus and Hydrobryum (Podostemaceae, Podostemoideae) with implications for their biogeography in East Asia. Syst Bot 29:921–932CrossRefGoogle Scholar
  28. Kitagawa T, Jeon S-R, Kitagawa E, Yoshioka M, Kashiwagi M, Okazaki T (2005) Genetic relationships among the Japanese and Korean striated spined loach complex (Cobitidae: Cobitis) and their phylogenetic positions. Ichthyol Res 52:111–122CrossRefGoogle Scholar
  29. Kitanishi S, Hayakawa A, Takamura K, Nakajima J, Kawaguchi Y, Onikura N, Mukai T (2016) Phylogeography of Opsariichthys platypus in Japan based on mitochondrial DNA sequences. Ichthyol Res 63:506–518CrossRefGoogle Scholar
  30. Kocher TD, Stepien CA (1997) Molecular systematics of fishes. Academic Press, New YorkGoogle Scholar
  31. Kottelat M (2001) Fishes of Laos. WHT Publications (Pte.) Ltd, ColomboGoogle Scholar
  32. Li X, Li J (1997) The Tanaka-Kaiyong Line-an important floristic line for the study of the flora of East Asia. Ann Mo Bot Gard 84:888–892CrossRefGoogle Scholar
  33. Li C, Ortí G (2007) Molecular phylogeny of Clupeiformes (Actinopterygii) inferred from nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 44:386–398CrossRefGoogle Scholar
  34. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  35. Lindberg GU (1972) Large-scale fluctuations of sea level in the Quaternary period: hypothesis based on biogeographical evidence. Nauka, LeningradGoogle Scholar
  36. Liu H, Yang J, Tang Q (2010) Estimated evolutionary tempo of East Asian gobionid fishes (Teleostei: Cyprinidae) from mitochondrial DNA sequence data. Chin Sci Bull 55:1501–1510CrossRefGoogle Scholar
  37. López JA, Chen WJ, Ortí G (2004) Esociform phylogeny. Copeia 2004:449–464CrossRefGoogle Scholar
  38. Maekawa K, Nalepa CA (2011) Biogeography and phylogeny of wood-feeding cockroaches in the genus Cryptocercus. Insect 2:354–368CrossRefGoogle Scholar
  39. Maruyama T, Fujii K, Kijima T, Maeda H (1987) Introductory process of foreign new fish species. Fisheries Agency, TokyoGoogle Scholar
  40. Matsuzawa Y, Senou H (2008) Alien fishes of Japan. Bun-ichi, TokyoGoogle Scholar
  41. Miura T (1966) Ecological notes of the fishes and the interspecific relations among them in Lake Biwa. Jpn J Limnol 27:49–72CrossRefGoogle Scholar
  42. Motokawa M, Kajihara H (2017) Species diversity of animals in Japan, diversity and commonality in animals. Springer, TokyoCrossRefGoogle Scholar
  43. Nakajima J, Nakagawa M (2007) Spawning season of the Chinese false gudgeon, Abbottina rivularis, in Katada Naiko, Lake Biwa. Humans and Nature 17:13–18Google Scholar
  44. Nakajima J, Onikura N, Matsui S, Oikawa S (2006) Geographical distribution of genuine freshwater fishes in Fukuoka Prefecture, northern Kyushu, Japan. Jpn J Ichthyol 53:117–131Google Scholar
  45. Nakamura M (1969) Cyprinid fishes of Japan. Studies on the life history of cyprinid fishes of Japan. Research Institute for Natural Resources, TokyoGoogle Scholar
  46. Neely DA, Perez MHS, Mendsaikhan B (2008) First Records of Rhinogobius lindbergi (Teleostei: Gobiidae) and Abbottina rivularis (Teleostei: Cyprinidae) in the Lake Buyr Drainage, Mongolia. J Great Lakes Res 34:334–341CrossRefGoogle Scholar
  47. Nishimura S (1980) Formation of the Sea of Japan. Tsukiji-Shokan, TokyoGoogle Scholar
  48. Okazaki T, Jeon S-R, Kitagawa T (2002) Genetic differentiation of piscivorous chub (genus Opsariichthys) in Japan, Korea and Russia. Zool Sci 19:601–610CrossRefGoogle Scholar
  49. Ota H (1998) Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Popul Ecol 40:189–204CrossRefGoogle Scholar
  50. Palumbi S, Martin A, Romano S, McMillian WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. University of Hawaii, HonoluluGoogle Scholar
  51. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  52. Qin Y, Li F, Tang B, Milliman JD (1986) Buried paleoriver system in western part of the South Huang Sea. Chin Sci Bull 31:1887–1889Google Scholar
  53. Qiu SW, Wang XK, Zhang SQ, Liang Y, Zhang ZQ, Zhu JH (2012) The evolution of the large paleolake in Songliao Plain and its formation. Quatern Sci 32:1011–1021Google Scholar
  54. Rambaut A (2016) FigTree Version 1.4.3. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 23 March 2017
  55. Rambaut A, Suchard MA, Xie D, Drummond AJ (2013) Tracer v1.6, Available from http://beast.bio.ed.ac.uk/Tracer. Accessed 3 August 2013
  56. Rohlf F J (1973) Algorithm 76. Hierarchical clustering using the minimum spanning tree. Comput J 16:93–95Google Scholar
  57. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  58. Rüber L, Kottelat M, Tan HH, Ng PKL, Britz R (2007) Evolution of miniaturization and the phylogenetic position of Paedocypris, comprising the world’s smallest vertebrate. BMC Evol Biol 7:38CrossRefGoogle Scholar
  59. Sasaki T, Kartavtsev YP, Chiba SN, Uematsu T, Sviridov VV, Hanzawa N (2007) Genetic divergence and phylogenetic independence of Far Eastern species in subfamily Leuciscinae (Pisces: Cyprinidae) inferred from mitochondrial DNA analyses. Genes Genet Syst 82:329–340CrossRefGoogle Scholar
  60. Shih HT, Suzuki H (2008) Taxonomy, phylogeny, and biogeography of the endemic mudflat crab Helice/Chasmagnathus complex (Crustacea: Brachyura: Varunidae) from East Asia. Zool Stud 47:114–125Google Scholar
  61. Shirai SM, Yabumoto Y, Kim I, Zhang C (2003) Phylogeny of sinipercid fishes and their relatives inferred from mtDNA cytochrome b gene: a preliminary study. Bull Kitakyushu Mus Ser A1:45–49Google Scholar
  62. Statistics Department, Ministry of Agriculture, Forestry, and Fisheries of Japan. (2000) The 10th fisheries census. AAFS, TokyoGoogle Scholar
  63. Swofford DL (2002) PAUP* 4.0b10a: phylogenetic analysis using parsimony (and other methods). Sinauer, SunderlandGoogle Scholar
  64. Takada M, TachiharaK, Kon T, Yamamoto G, Iguchi KI, Miya M, Nishida M (2010) Biogeography and evolution of the Carassius auratus-complex in East Asia. BMC Evol Biol 10:7.  https://doi.org/10.1186/1471-2148-10-7 CrossRefGoogle Scholar
  65. Takehana Y, Uchiyama S, Matsuda M, Jeon S-R, Sakaizumi M (2009) Geographic variation and diversity of the cytochrome b gene in wild populations of Medaka (Oryzias latipes) from Korea and China. Zool Sci 21:483–491CrossRefGoogle Scholar
  66. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  67. Tang WJ, He DK (2015) Investigation on alien fishes in Qinghai Province, China (2001–2014). J Lake Sci 27:502–510CrossRefGoogle Scholar
  68. Tang Q, Liu H, Mayden R, Xiong B (2006) Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Mol Phylogenet Evol 39:347–357CrossRefGoogle Scholar
  69. Tominaga K, Nakajima J, Watanabe K (2016) Cryptic divergence and phylogeography of the pike gudgeon Pseudogobio esocinus (Teleostei: Cyprinidae): a comprehensive case of freshwater phylogeography in Japan. Ichthyol Res 63:79–93CrossRefGoogle Scholar
  70. Tsukahara H (1954) Breeding habits of the fresh-water sucker, Abbottina rivularis (Basilewsky). Jpn J Ichthyol 3:139–143Google Scholar
  71. Vidthayanon C, Kottelat M (1995) First record of Abbottina rivularis (Cyprinidae: Gobioninae) from the Mekong Basin. Jpn J Ichthyol 41:463–465Google Scholar
  72. Watanabe K (2012) Faunal structure of Japanese freshwater fishes and its artificial disturbance. Environ Biol Fishes 94:533–547CrossRefGoogle Scholar
  73. Watanabe K, Takahashi H (2010) Natural history of freshwater fish biogeography (Tansuigyo-chiri no shizenshi). Hokkaido University Press, SapporoGoogle Scholar
  74. Watanabe K, Iguchi K, Hosoya K, Nishida M (2000) Phylogenetic relationships of the Japanese minnows, Pseudorasbora (Cyprinidae), as inferred from mitochondrial 16S rRNA gene sequences. Ichthyol Res 47:43–50CrossRefGoogle Scholar
  75. Watanabe K, Takahashi H, Kitamura A, Yokoyama R, Kitagawa T, Takeshima H, Sato S, Yamamoto S, Takehana Y, Mukai T, Ohara K, Iguchi K (2006) Biogeographical history of Japanese freshwater fishes: phylogeographic approaches and perspectives. Jpn J Ichthyol 53:1–38Google Scholar
  76. Watanabe K, Abe T, Iwata A (2009) Phylogenetic position and generic status of the Japanese botiid loach. Ichthyol Res 56:421–425CrossRefGoogle Scholar
  77. Watanabe K, Kawase S, Mukai T, Kakioka R, Miyazaki J-I, Hosoya K (2010a) Population divergence of Biwia zezera (Cyprinidae: Gobioninae) and the discovery of a cryptic species, based on mitochondrial and nuclear DNA sequence analyses. Zool Sci 27:647–655CrossRefGoogle Scholar
  78. Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2010b) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109CrossRefGoogle Scholar
  79. Watanabe K, Mori S, Tanaka T, Kanagawa N, Itai T, Kitamura J, Suzuki N, Tominaga K, Kakioka R, Tabata R, Abe T, Tashiro Y, Hashimoto Y, Nakajima J, Onikura N (2014) Genetic population structure of Hemigrammocypris rasborella (Cyprinidae) inferred from mtDNA sequences. Ichthyol Res 61:352–360CrossRefGoogle Scholar
  80. Watanabe K, Tominaga K, Nakajima J, Kakioka R, Tabata R (2017) Japanese freshwater fishes: biogeography and cryptic diversity. In: Motokawa M, Kajihara H (eds) Species diversity of animals in Japan, diversity and commonality in animals. Springer, Tokyo, pp 183–227CrossRefGoogle Scholar
  81. Watanabe K, Sakai H, Sanada T, Nishida M (2018) Comparative phylogeography of diadromous and freshwater daces of the genus Tribolodon (Cyprinidae). Ichthyol Res 65:383–397CrossRefGoogle Scholar
  82. Xia X, Zhang X, Liu H (2005) Phylogeography and speciation of Pseudogobio vaillanti in China: deep molecular divergence in the absence of morphological change. Prog Nat Sci 15:1064–1069CrossRefGoogle Scholar
  83. Xiao W, Zhang Y, Liu H (2001) Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Mol Phylogenet Evol 18:163–173CrossRefGoogle Scholar
  84. Xu W, Yin W, Chen A, Li J, Lei G, Fu C (2014) Phylogeographical analysis of a cold-temperate freshwater fish, the Amur sleeper (Perccottus glenii) in the Amur and Liaohe River basins of northeast Asia. Zool Sci 31:671–679CrossRefGoogle Scholar
  85. Yamamoto G, Takada M, Iguchi K, Nishida M (2010) Genetic constitution and phylogenetic relationships of Japanese crucian carps (Carassius). Ichthyol Res 57:215–222CrossRefGoogle Scholar
  86. Yang J, He S, Freyhof J, Witte K, Liu H (2006) The phylogenetic relationships of the Gobioninae (Teleostei: Cyprinidae) inferred from mitochondrial cytochrome b gene sequences. Hydrobiologia 553:255–266CrossRefGoogle Scholar
  87. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237CrossRefGoogle Scholar
  88. Zhang H, Yan J, Zhang G, Zhou K (2008) Phylogeography and demographic history of Chinese black-spotted frog populations (Pelophylax nigromaculata): evidence for independent refugia expansion and secondary contact. BMC Evol Biol 8:21.  https://doi.org/10.1186/1471-2148-8-21 CrossRefGoogle Scholar

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© The Ichthyological Society of Japan 2019

Authors and Affiliations

  1. 1.Department of Zoology, Division of Biological Sciences, Graduate School of ScienceKyoto UniversitySakyoJapan
  2. 2.Institute of ZoologyChinese Academy of SciencesBeijingChina
  3. 3.Fukuoka Institute of Health and Environmental SciencesDazaifuJapan
  4. 4.Fishery Research LaboratoryKyushu UniversityFukutsuJapan
  5. 5.Conservation and Research CenterTaipeiTaiwan
  6. 6.Kwansei Gakuin Senior High SchoolNishinomiyaJapan

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