Advertisement

Conservation Genetics

, Volume 19, Issue 5, pp 1025–1038 | Cite as

Phylogeography of Eleotris fusca (Teleostei: Gobioidei: Eleotridae) in the Indo-Pacific area reveals a cryptic species in the Indian Ocean

  • Marion I. Mennesson
  • Céline Bonillo
  • Eric Feunteun
  • Philippe Keith
Research Article
  • 145 Downloads

Abstract

Indo-Pacific insular freshwater systems are mainly dominated by amphidromous species. Eleotris fusca is a widespread one, its life cycle is characterised by a marine pelagic larval phase allowing the species to disperse in the ocean and then to recruit to remote island rivers. In the present study, the population structure of E. fusca over its Indo-Pacific distribution range (Western Indian Ocean to French Polynesia, Pacific Ocean) was evaluated. We analysed a section of mitochondrial COI of 557 individuals sampled from 28 islands to visualise the population structure. Haplotypes diversity (Hd) was between 0.458 and 1 and, nucleotide diversity (π) was between 0.001 and 0.02. Two distinct genetic groups appeared, one in the Indian Ocean and the other in the Pacific Ocean (FST mean = 0.901; 5.2% average divergence). Given these results, complete mitogenomes (mtDNA) were sequenced and combined with the nuclear Rhodopsin (Rh) gene for a subset of individuals. The two phylogenetic trees based on each analysis showed the same genetic pattern: two different groups belonging to the Indian and the Pacific oceans (6.6 and 1.6% of divergence for mtDNA and Rh gene respectively), which supported species level differentiation. These analyses revealed the presence of two sister species confounded until present under the name of Eleotris fusca. One of them is cryptic and endemic of the Indian Ocean and the other one is the true E. fusca, which keeps, nevertheless, its status of widespread species.

Keywords

Freshwater fish Amphidromous Complete mitogenome Nuclear gene 

Notes

Acknowledgements

The study was made possible by a grant given to the French Ichthyological Society in the context of the ‘Critical Ecosystem Partnership Fund (CEPF)’ (Melanesia hotspot). The Critical Ecosystem Partnership Fund is a joint initiative of l’Agence Française de Développement, Conservation International, the Global Environment Facility, the Government of Japan, the MacArthur Foundation and the World Bank. A fundamental goal is to ensure civil society is engaged in biodiversity conservation. For the Seychelles, we would like to thank the UNDP and particularly E. Henriette and B. Santerre. Thanks to R. Fanchette, Ministry of Environment and Energy, Wildlife, Trade and Conservation section. For the Comoros, we would like to thank Yahaya Ibrahim (CNDRS), for Madagascar, J. Aride from Madagascar National Parks the Manager of Masoala National Parc and the DIAMSOI team. For Reunion and Mayotte, we thank the Environnement Office, the Agriculture Office, and ARDA. For the Solomon Islands, we would like to acknowledge the customary landowners, villages and tribes, ESSI and the Solomon Islands’ Government. For Vanuatu, we would like to acknowledge the Department of Environmental Protection and Conservation and D. Kalfatak. For Samoa, we acknowledge the Samoan Ministry of Natural Resources Environment and Meteorology and Conservation International. For the Cook Islands, we would like to thank the Office of the Prime Minister. For French Polynesia, we want to thank the Research Delegation (especially J.Y. Meyer), and the Environment Delegation. For the loan of specimens, we thank: P. Pruvost, R. Causse, Z. Gabsi, C. Ferrara, M. Hautecœur (MNHN). Finally, we would like to thank the “Service de systématique moléculaire” of the MNHN (CNRS UMS 2700) for the laboratory access and the assistance provided.

Supplementary material

10592_2018_1063_MOESM1_ESM.xlsx (16 kb)
Supplementary Table 8 The percentage of differences between sequences (above diagonal) and the number of bases (below diagonal), which are not identical for the complete mtDNA. Differences between E. cf. fusca and E. fusca are highlighted in bold type (XLSX 16 KB)
10592_2018_1063_MOESM2_ESM.xlsx (50 kb)
Supplementary Table 9 The percentage of differences between sequences (above diagonal) and the number of bases (below diagonal), which are not identical for the Rh gene. Differences between E. cf. fusca and E. fusca are highlighted in bold type (XLSX 50 KB)

References

  1. Abdou A (2016) Amphidromie et phylogéographie des Neritidae amphidromes de l’Indo-Pacifique. PhD dissertation, EPHE, PerpignanGoogle Scholar
  2. Abdou A, Keith P, Galzin R (2015) Freshwater neritids (Mollusca: Gastropoda) of tropical islands, amphidromy as a life cycle, a review. Revue d’Ecologie (Terre et Vie) 70:387–397Google Scholar
  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein dataset search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the Coral Triangle. Evolution 60:1825–1839CrossRefPubMedGoogle Scholar
  6. Borkin IV (1991) Ichthyoplankton of western Spitzbergen coastal waters. J Ichthyol 31:680–685Google Scholar
  7. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  8. Castelin M, Feutry P, Hautecoeur M, Marquet G, Wowor D, Zimmermann G, Keith P (2013) New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (Fabricius, 1789) (Crustacea: Decapoda : Palaeminidae). Mar Biol.  https://doi.org/10.1007/s00227-013-2191-y CrossRefGoogle Scholar
  9. Chen WJ, Bonillo C, Lecointre G (2003) Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol Phyl Evol 26:262–288CrossRefGoogle Scholar
  10. Coleman RR, Eble JA, Dibatiista JD, Rocha LA, Randall JE (2016) Regal phylogeography: Range-wide survey of the marine angelfish Pyroplites diacanthus reveals evolutionary partitions between the Red Sea, Indian Ocean, and the Pacific Ocean. Mol Phyl Evol 100:243–253CrossRefGoogle Scholar
  11. Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626CrossRefPubMedGoogle Scholar
  12. De Bruyn M, Mather PB (2007) Molecular signatures of Pleistocene sea-level changes that affected connectivity among freshwater shrimp in Indo-Australian waters. Mol Ecol 16:4295–4307CrossRefPubMedGoogle Scholar
  13. De Bruyn M, Wilson JA, Mather PB (2004) Huxley’s line demarcates extensive genetic divergences between eastern and western forms of the giant freshwater prawn, Macrobrachium rosenbergii. Mol Phyl Evol 30:251–257CrossRefGoogle Scholar
  14. Dettai A, Lautredou AC, Bonillo C, Goimbault E, Busson F, Causse R, Couloux A, Cruaud C, Duhamel G, Denys G (2011) The Actinopterygian diversity of the CEAMARC cruises: barcoding and molecular taxonomy as a multi-level tool for new findings. Deep Sea Res II 58:250–263CrossRefGoogle Scholar
  15. Dibattista JD, Wilcox C, Craig MT, Rocha LA, Bowen BW (2011) Phylogeography of the Pacific Blueline Surgeonfish, Acanthurus nigroris, reveals high genetic connectivity and a cryptic endemic species in the Hawaiian Archipelagos. J Mar Biol Article ID 839134:1–17.  https://doi.org/10.1155/2011/839134 CrossRefGoogle Scholar
  16. Ekman S (1953) Zoogeography of the sea. Sidgwick and Jackson, LondonGoogle Scholar
  17. 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. Genetic 131:479–491Google Scholar
  18. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  19. Feutry P, Vergnes A, Broderick D, Lambourdiere J, Keith P (2013) Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo-Pacific diadromous fish (Kuhlia rupestris)? Mol Ecol 22:1518–1530CrossRefPubMedGoogle Scholar
  20. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  21. Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648CrossRefGoogle Scholar
  22. Gaither MR, Toonen R, Robertson D, Planes S, Bowen BW (2010) Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). J Biogeogr 37:133–147CrossRefGoogle Scholar
  23. Gaither M, Bowen B, Bordenave T, Rocha L, Newman SJ, Gomez J, Herwerden L, Craig M (2011) Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle. BMC Evol Biol 11:189.  https://doi.org/10.1186/1471-2148-11-189 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  25. Hare JA, Cowen RK (1996) Transport mechanisms of larval and pelagic juvenile bluefish (Pomatomus saltarix) from South Atlantic Bight spawning grounds to Middle Atlantic Bight nursery habitats. Limnol Oceanogr 41:1264–1280CrossRefGoogle Scholar
  26. Hinsinger DD, Debruyne R, Thomas M, Denys GP, Mennesson M, Utge J, Dettai A (2015) Fishing for barcoding in the Torrent: from COI to complete mitogenomes on NGS platforms. DNA Barcodes 3:170–186CrossRefGoogle Scholar
  27. IUCN France, MNHN, SEOR, ARDA, Insectarium de La Réunion, GLOBICE and Kélonia (2013) La liste rouge des espèces menacées en France - Faune de la Réunion. Paris, France. http://www.uicn.fr/Liste-rouge-faune-Reunion.html
  28. Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, Sado T, Mabuchi K, Takeshima H, Miya M, Nishida M (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol And Evol 30:2531–2540CrossRefGoogle Scholar
  29. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  30. Keith P (2003) Biology and ecology of amphidromous Gobiidae in the Indo-Pacific and the Caribbean regions. J Fish Biol 63:831–847CrossRefGoogle Scholar
  31. Keith P, Lord C (2011) Tropical freshwater gobies: amphidromy as a life cycle. In: The biology of Gobies, Science Publishers & CRC Press, pp 243–277Google Scholar
  32. Keith P, Lord C, Vigneux E (2006) In vivo observations on post-larval development of freshwater gobies and eleotrids from French Polynesia and New Caledonia. Ichthyol Explor Freshw 17:187–191Google Scholar
  33. Keith P, Hoareau TB, Lord C, Ah-Yane O, Gimmoneau G, Robinet T, Valade P (2008) Characterisation of post-larval to juvenile stages, metamorphosis and recruitments of an amphidromous goby, Sicyopterus lagocephalus (Pallas) (Teleostei: Gobiidae: Sicydiinae). Mar freshwater Res 59:876–889CrossRefGoogle Scholar
  34. Keith P, Marquet G, Lord C. Kalfatak D, Vigneux E (2010) Poissons et crustacés d’eau douce du Vanuatu. Société Française d’Ichtyologie, Paris, p 253Google Scholar
  35. Keith P, Marquet G, Gerbeaux P, Vigneux E, Lord C (2013) Poissons et crustacés d’eau douce de Polynésie. Société Française d’Ichtyologie, Paris, p 282Google Scholar
  36. Keith P, Lord C, Maeda K (2015) Indo-Pacific Sicydiine Gobies: biodiversity, life traits and conservation. Société Française d’Ichtyologie, Paris, p 256Google Scholar
  37. Keyse J, Crandall E, Toonen RJ, Meyer CP, Treml EA, Riginos C (2014) The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities in the region. Bull Mar Sci 90:47–78CrossRefGoogle Scholar
  38. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX et al (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200CrossRefPubMedGoogle Scholar
  39. Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701CrossRefPubMedGoogle Scholar
  40. Lord C, Lorion J, Dettai A, Watanabe S, Tsukamoto K, Cruaud C, Keith P (2012) From endemism to widespread distribution: phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae). Mar Ecol Prog Ser 455:269–285CrossRefGoogle Scholar
  41. Ludt WB, Rocha LA (2015) Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J Biogeogr 42:25–38CrossRefGoogle Scholar
  42. Maeda K, Tachihara K (2004) Instream distributions and feeding habits of two species of sleeper, Eleotris acanthopoma and Eleotris fusca in the Teima River, Okinawa Island. Ichthyol Res 51:233–240CrossRefGoogle Scholar
  43. Maeda K, Tachihara K (2006) Fish fauna in the Teima Stream, Okinawa Island. Biol Mag Okinawa 44:7–25Google Scholar
  44. McDowall RM (1992) Diadromy: origins and definition of terminology. Copeia 1:248–251CrossRefGoogle Scholar
  45. McDowall RM, Mitchell CP, Brothers EB (1994) Age at migration from the sea of juvenile Galaxias in New Zealand (Pisces: Galaxiidae). Bull Mar Sci 54:385–402Google Scholar
  46. Mennesson MI, Keith P (2017) Evidence of two species currently under the name of Eleotris fusca (Gobioidei: Eleotridae) in the Indian Ocean. Cybium 41:213–220Google Scholar
  47. Mennesson MI, Tabouret H, Pécheyran C, Feunteun E, Keith P (2015) Amphidromous life cycle of Eleotris fusca (Gobioidea: Eleotridae), a widespread species from the Indo-Pacific studied by otolith analysis. Cybium 39:249–260Google Scholar
  48. Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phyl Evol 26:121–138CrossRefGoogle Scholar
  49. Mirams AGK, Treml EA, Shields JL, Liggins L, Riginos C (2011) Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge. Coral Reefs 30:937–949CrossRefGoogle Scholar
  50. Murphy CA, Cowan JHJR. (2007) Production, marine larval retention or dispersal, and recruitment of amphidromous Hawaiian gobioids: issues and implications. In: Evenhuis NL, Fitzsimons JM, Biology of Hawaiian Streams and Estuaries. Bishop Museum Bulletin in Cultural Environmental Studies vol 3, pp 63–74Google Scholar
  51. Myers GS (1949) Usage of anadromous, catadromous and allied terms for migratory fishes. Copeia 2:89–97CrossRefGoogle Scholar
  52. Nelson SG, Parham JE, Tibatts RB, Camacho FA, Lebere T, Smith BD (1997) Distribution and microhabitats of the amphidromous gobies in streams of Micronesia. Micronesica 30:83–91Google Scholar
  53. Planes S (1993) Genetic differentiation in relation to restricted larval dispersal of the convict surgeonfish Acanthurus triostegus in French Polynesia. Mar Ecol 98:237–246CrossRefGoogle Scholar
  54. Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Soc Study Evol 56:378–399Google Scholar
  55. Pous S, Feunteun E, Ellien C (2010) Investigation of tropical eel spawning area in the south-western indian ocean: influence of the oceanic circulation. Prog Oceanogr 86:396–413CrossRefGoogle Scholar
  56. Rambaut A (2007) FigTree v1.3.1. Available at http://tree.bio.ed.ac.uk/software/figtree/
  57. Rambaut A, Drummond AJ (2007) Tracer v1.4, Available at http://beast.bio.ed.ac.uk/Tracer
  58. Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Ho ̈hna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:1–4CrossRefGoogle Scholar
  59. Sathiamurthy E, Voris HK (2006) Maps of Holocene sea level transgression and submerged lakes on the Sunda Shelf. Nat Hist J Chulalongkorn Univ 2:1–43Google Scholar
  60. Spalding MD, Fox HE, Halpern BS, McManus MA, Molnar J, Allen GR, Davidson N, Jorge ZA, Lombana AL, Lourie SA et al (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583CrossRefGoogle Scholar
  61. Szabó Z, Smelgrove B, Craig MT, Rocha LA, Bowen BW (2014) Phylogeography of the manybar goatfish, Parupeneus multifasciatus, reveals isolation of the Hawaiian Archipelago and a cryptic species in the Marquesas Islands. Bull Mar Sci 90:493–512CrossRefGoogle Scholar
  62. Taillebois L, Castellin M, Ovenden JR, Bonillo C, Keith P (2013) Contrasting genetic structure among populations of two amphidromous fish species (Sicydiinae) in the Central West Pacific. Plos ONE 8:e75465CrossRefPubMedPubMedCentralGoogle Scholar
  63. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  64. Watson RE, Keith P, Marquet G (2007) Akihito vanuatu, a new genus and new species of freshwater goby from the South Pacific (Teleostei: Gobioidei: Sicydiinae). Cybium 31:341–349Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Muséum national d’Histoire naturelle, UMR 7208 BOREA (MNHN-CNRS-Sorbonne Université-IRD-UCBN-UA)Paris Cedex 05France
  2. 2.Département Systématique et Evolution, UMS 2700 “Outils et Méthodes de la Systématique Intégrative” MNHN-CNRS, Service de Systématique Moléculaire, Muséum national d’Histoire naturelleParis Cedex 05France

Personalised recommendations