Time-calibrated molecular phylogeny reveals a Miocene–Pliocene diversification in the Amazon miniature killifish genus Fluviphylax (Cyprinodontiformes: Cyprinodontoidei)

Abstract

Species of Fluviphylax are widely distributed over the Amazon and Orinoco river drainages and are among the smallest fish in the neotropics, inhabiting areas near the margin of slow-flowing clear and black water streams and lakes. Here, we present the first multigene molecular phylogeny of Fluviphylax, including all five nominal species of Fluviphylax and three undescribed species. The analysis included fragments of one mitochondrial and five nuclear genes, totaling 5880 bp. The dataset was analyzed using maximum parsimony, maximum likelihood, and Bayesian inference approaches providing high-supported well-solved trees. A time-calibrated analysis was performed providing information on the origin and diversification of the miniature genus in the Amazon. We estimate that Fluviphylax lineage splits from its sister group, the Anablepidae and Poeciliidae (Poeciliinae sensu Parenti, 1981), during the Late Eocene, about 36.6 Mya; but lineage diversification started only in the Middle Miocene, about 16 Mya, during the formation of the Pebas system. Subsequent splits within Fluviphylax occurred in the Late Miocene–Pliocene, between 10 and 6 Mya and during the Pliocene, and were probably influenced by paleogeographical events such as the breaching of the Purus arch, the rise of the Vaupés arch, the uplift of the Fitzcarrald arch, and the capture of the Contigo and Uraricoera river drainages by the Branco River. The present time-calibrated analysis provides the first insight on the evolution of one of the smallest vertebrate taxa in the Amazon and Orinoco river drainages.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Arrington, D. A., & Winemiller, K. O. (2003). Diel changeover in sand-beach fish assemblages in a neotropical floodplain river. Journal of Fish Biology, 63, 442–459.

    Article  Google Scholar 

  2. Arrington, D. A., & Winemiller, K. O. (2006). Habitat affinity, the seasonal flood pulse, and community assembly in littoral zone of a neotropical floodplain river. Journal of the North American Benthological Society, 25(1), 126–141.

    Article  Google Scholar 

  3. Bloom, D. D. & Lovejoy, N. R. (2011). The biogeography of marine incursions in South America. In J. S. Albert & R. E. Reis (Eds.), Historical Biogeography of Neotropical Freshwater Fishes (pp. 137–144). The Regents of the University of California.

  4. Bragança, P. H. N., Amorim, P. F., & Costa, W. J. E. (2018). Pantanodontidae (Teleostei, Cyprinodontiformes), the sister group to all other cyprinodontoid killifishes as inferred by molecular data. Zoosystematics and Evolution, 94(1), 137–145.

    Article  Google Scholar 

  5. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., & Thompson, J. D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research., 31(13), 3497–3500.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Costa, W. J. E. M. (1996). Relationships, monophyly and three new species of the neotropical miniature poeciliid genus Fluviphylax (Cyprinodontiformes: Cyprinodontoidei). Ichthyological Exploration of Freshwaters, 7(2), 111–130.

    Google Scholar 

  7. Costa, W. J. E. M., & Le Bail, P. Y. (1999). Fluviphylax palikur: a new Poeciliid from the Rio Oiapoque basin, Northern Brazil (Cyprinodontiformes: Cyprinodontoidei), with comments on miniaturization in Fluviphylax and other neotropical freshwater fishes. Copeia, 1999, 1027–1034.

    Article  Google Scholar 

  8. Costa, W. J. E. M., Amorim, P. F., & Mattos, J. L. O. (2017). Molecular phylogeny and timing of diversification in South American Cynolebiini seasonal killifishes. Molecular Phylogenetics and Evolution, 116, 61–68.

    Article  PubMed  Google Scholar 

  9. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Dias de Gamero, M. L. (1996). The changing course of the Orinoco River during the Neogene: a review. Palaeogeography, Palaeoclimatology, Palaeoecology, 123, 385–402.

    Article  Google Scholar 

  11. Donoghue, P. C. J., & Benton, M. J. (2007). Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends in Ecology and Evolution, 22(8), 424–431.

    Article  PubMed  Google Scholar 

  12. Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoSBiology., 4, 699–710.

    CAS  Google Scholar 

  13. Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Espurt, N., Baby, P., Brusset, S., Roddaz, M., Hermoza, W., Regard, V., Antoine, P. -O., Salas-Gismondi, R., & Bolaños, R. (2007). How does the Nazca Ridge subduction influence the modern Amazonian foreland basin? Geology, 35, 515–518.

  15. Espurt, N., Baby, P., Brusset, S., Roddaz, M., Hermoza, W., & Barbarand, J. (2010). The Nazca Ridge and uplift of the Fitzcarrald arch: implications for regionalgeology in northern South America. In C. Hoorn, & F.P. Wesselingh (Eds.), Amazonia, Landscape and Species Evolution: A Look into the Past ( pp. 89–100). Blackwell: London.

  16. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39(4), 783–791.

    Article  PubMed  Google Scholar 

  17. Ferreira, E. J. G., Zuanon, J., Forsberg, B., Goulding, M., & Briglia-Ferreira, R. (2007). Rio Branco: Peixes, ecologia e conseração de Roraima. Amazon Conservation Association/Instituto Nacional de Pesquisas da Amazônia/Sociedade Civil Mamirauá: Manaus.

  18. Figueiredo, J., Hoorn, C., van der Ven, P., & Soares, E. (2009). Late Miocene onset of the Amazon River and the Amazon deep-sea fan: evidence from the Foz do Amazonas basin. Geology, 37, 619–622.

    Article  Google Scholar 

  19. Figueiredo, J., Hoorn, C., van der Ven, P., & Soares, E. (2010). Late Miocene onset of the Amazon River and the Amazon deep-sea fan: evidence from the Foz do Amazonas basin: Reply. Geology, 38, 213.

    Article  Google Scholar 

  20. Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294–299.

    PubMed  CAS  Google Scholar 

  21. Gernhard, T. (2008). The conditioned reconstruction process. Journal of Theoretical Biology, 253(4), 769–778.

    Article  PubMed  Google Scholar 

  22. Ghedotti, M. J. (1998). Phylogeny and classification of the Anablepidae (Teleostei: Cyprinodontiformes). In L. R. Malabarba, R. E. Reis, R. P. Vari, Z. M. S. Lucena, & C. A. S. Lucena (Eds.), Phylogeny and Classification of Neotropical Fishes (pp. 561–582). Edipucrs: Porto Alegre.

    Google Scholar 

  23. Ghedotti, M. J. (2000). Phylogenetic analysis and taxonomy of the poecilioid fishes (Teleostei: Cyprinodontiformes). Zoological Journal of the Linnean Society, 130, 1–53.

    Article  Google Scholar 

  24. Goulding, M., Leal-Carvalho, M., & Ferreira, E. (1988). Rio Negro, rich life in poor water. Amazonian diversity and foodchain ecology as seen through fish communities. the Netherlands: SPB Academic Publishing.

    Google Scholar 

  25. Helmstetter, A. J., Papadopulos, A. S. T., Igea, J., Van Dooren, T. J. M., Leroi, A. M., & Savolainen, V. (2016). Viviparity stimulates diversification in an order of fish. Nature Communications, 7, 11271. https://doi.org/10.1038/ncomms11271.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Ho, S. Y. W. (2014). The changing face of the molecular evolutionary clock. Trends in Ecology & Evolution, 29, 496–503.

    Article  Google Scholar 

  27. Hoorn, C. (1993). Marine incursions and the influence of Andean tectonics on the Miocene depositional history of northwestern Amazonia: results of a palynostratigraphic study. Palaeogeography, Palaeoclimatology, Palaeoecology, 105, 267–309.

    Article  Google Scholar 

  28. Hoorn, C. (1994). Fluvial palaeoenvironments in the intracratonic Amazonas Basin (Early Miocene-early Middle Miocene, Colombia). Palaeogeography, Palaeoclimatology, Palaeoecology, 109, 1–54.

    Article  Google Scholar 

  29. Hoorn, C., Guerrero, J., Sarmiento, G. A., & Lorente, M. A. (1995). Andean tectonics as a cause for changing drainage patterns in Miocene northern South America. Geology, 23, 237–240.

    Article  Google Scholar 

  30. Hoorn, C., Wesselingh, F. P., Hovikoski, J., & Guerrero, J. (2010). The development of the Amazonian mega-wetland (Miocene; Brazil, Colombia, Peru, Bolivia). In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, Landscape and Species Evolution: A Look into the Past (pp. 123–142). Blackwell: London.

    Google Scholar 

  31. Hrbek, T., Seckinger, J., & Meyer, A. (2007). A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Molecular Phylogenetics and Evolution, 43, 986–998.

    Article  PubMed  CAS  Google Scholar 

  32. Hubert, N., & Renno, J. F. (2006). Historical biogeography of South America freshwater fishes. Journal of Biogeography, 33, 1414–1436.

    Article  Google Scholar 

  33. Jaramillo, C., Romero, I., D’Apolito, C., Bayona, G., Duarte, W., Louwye, S., Escobar, J., Luque, J., Carrillo-Briceño, J. D., Zapata, V., Mora, A., Schouten, S., Zavada, M., Harrington, G., Ortiz, J., & Wesselingh, F. P. (2017). Miocene flooding events of western Amazonia. Science Advances, 3(5), e1601693. https://doi.org/10.1126/sciadv.1601693.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Lasso, C., Mojica, J. I., Usma, J. S., Maldonado-Ocampo, J. A., Do Nascimiento, C., Taphorn, D. C., et al. (2004). Peces de la cuenca del rio Orinoco. Parte L Lista de especies y distribucion por subcuencas. Biota Colombiana, 5(2), 95–158.

    Google Scholar 

  35. Li, C., Ortí, G., Zhang, G., & Lu, G. (2007). A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evolutionary Biology, 7, 44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. López, J. A., Chen, W. J., & Ortí, G. (2004). Esociform phylogeny. Copeia, 3, 449–564.

    Article  Google Scholar 

  37. Lovejoy, N. R., Albert, J. S., & Crampton, W. G. R. (2006). Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes. Journal of South American Earth Sciences, 21(1), 5–13.

    Article  Google Scholar 

  38. Lucinda, P. H. F. (2003). Family Poeciliidae. In R. E. Reis, S. O. Kullander, & C. J. Ferraris Jr. (Eds.), Check List of the Freshwater Fishes of South and Central America (pp. 555–581). Edipucrs: Porto Alegre.

    Google Scholar 

  39. Lujan, N. K. & Armbruster, J. W. (2011). The Guiana shield. In J. S. Albert, & R. E. Reis (Eds.), Historical Biogeography of Neotropical Freshwater Fishes (pp. 211–224). The Regents of the University of California.

  40. Lujan, N. K., Armbruster, J. W., Lovejoy, N. R., & Lopéz-Fernández, H. (2014). Multilocus molecular phylogeny of the suckermouth armored catfishes (Siluriformes: Loricariidae) with a focus on subfamily Hypostominae. Molecular Phylogenetics and Evolution, 82, 269–288.

    Article  PubMed  Google Scholar 

  41. Lundberg, J. G., Marshall, L. G., Guerrero, J., Horton., Malabarba, M. C. S. L., & Wesselingh, F. (1998). The stage for neotropical fish diversification: a history of tropical South American rivers. In L. R. Malabarba., R. E. Reis., R P, Vari, Z. M, Lucena, & C. A. S, Lucena (Eds.), Phylogeny and Classification of Neotropical Fishes (pp. 13–48). Edipucrs: Porto Alegre.

  42. Lundberg, J. G., Sabaj Pérez, M. H., Dahdul, W. M., Orangel, A., & Aguilera, S. (2010). The Amazonian Neogene fish fauna. In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, Landscape and Species Evolution: A Look into the Past (pp. 281–301). Blackwell: London.

    Google Scholar 

  43. Maldonado-Ocampo, J. A., Vari, R. P., & Usma, J. S. (2008). Checklist of the freshwater fishes of Colombia. Biota Colombiana, 9(2), 143–237.

    Google Scholar 

  44. Montaña, C. G., Layman, C. A., & Taphorn, D. C. (2008). Comparison of fish assamblages in two littoral habitats in a neotropical Morichal stream in Venezuela. Neotropical Ichthyology, 6(4), 577–582.

    Article  Google Scholar 

  45. Myers, G. S., & Carvalho, A. (1955). Notes on the classification and names of cyprinodont fishes. Tropical Fish Magazine, 4, 7.

    Google Scholar 

  46. Parenti, L. R. (1981). A phylogenetic and biogeographic analysis of cyprinodontiform fishes (Teleostei, Atherinomorpha). Bulletin of the American Museum of Natural History, 168, 335–357.

    Google Scholar 

  47. Parham, J. F., Donoghue, P. C., Bell, C. J., Galway, T. D., Head, J. J., Holroyd, P. A., et al. (2012). Best practices for justifying fossil calibrations. Systematic Biology, 62, 346–359.

    Article  Google Scholar 

  48. Pohl, M., Milvertz, F. C., Meyer, A., & Vences, M. (2015). Multigene phylogeny of cyprinodontiform fishes suggests continental radiations and a rougue taxon position of Pantanodon. Vertebrate Zoology, 65(1), 37–44.

    Google Scholar 

  49. Pollux, B. J. A., Meredith, R. W., Springer, M. S., Garland, T., & Reznick, D. N. (2014). The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature, 513, 233–236.

    Article  PubMed  CAS  Google Scholar 

  50. Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2013). Tracer, v1.5 http://beast.bio.ed.ac.uk/Trace.

  51. Reznick, D. N., Furness, A. I., Meredith, R. W., & Springer, M. S. (2017). The origin and biogeographic diversification of fishes in the family Poeciliidae. PLoSONE, 12(3), e0172546. https://doi.org/10.1371/journal.pone.0172546.

    Article  CAS  Google Scholar 

  52. Roberts, T. R. (1970). Description, osteology, and relationships of the Amazonian cyprinodont fish Fluviphylax pygmaeus. Breviora, 347, 1–28.

    Google Scholar 

  53. Roberts, T. R. (1972). Ecology of the fishes in the Amazon and Congo basins. Bulletin of the Museum of Comparative Zoolgy, 143, 117–147.

    Google Scholar 

  54. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Hohna, S., et al. (2011). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.

    Article  Google Scholar 

  55. Rosen, D. E. (1973). Suborder Cyprinodontoidei. In D.M. Cohen et al. (Eds.), Fishes of the western North Atlantic (pp. 229-262). Sears Foundation for Marine Research Memoir 1, Pt. 6, Yale University.

  56. Rosen, D. E., & Bailey, R. M. (1963). The poeciliid fishes (Cyprinodontiformes) – their structure, zoogeography and systematics. Bulletin of the American Museum of Natural History, 126, 1–176.

    Google Scholar 

  57. Schneider, C. H., Gross, M. C., Terencio, M. L., & Porto, J. I. R. (2012). Cryptic diversity in the mtDNA of the ornamental fish Carnegiella strigata. Journal of Fish Biology, 81(4), 1210–1224.

    Article  PubMed  CAS  Google Scholar 

  58. Swofford, D. L. (2003). PAUP* – Phylogenetic Analysis Using Parsi-mony (*and other methods) version 4b10. Sunderland, Massachusetts: Sinauer Associates.

    Google Scholar 

  59. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Weitzman, S. H., & Vari, R. P. (1988). Miniaturization in South America freshwater fishes: an overview and discussion. Proceedings of the Biological Society of Washington, 101, 444–465.

    Google Scholar 

  61. Wesselingh, F. P. & Hoorn, C. (2011). Geological development of the Amazon and Orinoco basins. In J.S. Albert & R.E. Reis (Eds.), Historical Biogeography of Neotropical Freshwater Fishes (pp. 59–67). The Regents of the University of California.

  62. Wesselingh, F. P., & Salo, J. (2006). A Miocene perspective on the evolution of the Amazoniana biota. Scripta Geologica, 133, 439–445.

    Google Scholar 

  63. Whitley, G. P. (1965). Some fish genera scrutinized. Proceedings of the Royal Zoological Society of New South Wales, 1964–65, 25–26.

    Google Scholar 

  64. Winemiller, K. O. & Willis, S. C. (2011). The Vaupes arch and Casiquiare Canal: barriers and passages. In J. S. Albert & R. E. Reis (Eds.), Historical Biogeography of Neotropical Freshwater Fishes (pp. 225–242). The Regents of the University of California.

  65. Winemiller, K. O., Lopéz-Fernández, H., Taphorn, D. C., Nico, L. G., & Barbarino Duque, A. (2008). Fish assemblages of the Casiquiare River, a corridor and zoogeographical filter for dispersal between the Orinoco and Amazon basins. Journal of Biogeography, 35(9), 1551–1563.

    Article  Google Scholar 

  66. Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D.dissertation, The University of Texas at Austin.

Download references

Acknowledgments

We are grateful to P. F. Amorim, E. Henschel, and F.P. Ottoni for the valuable help in several collecting expeditions, and to C. Gama and H. Lazzaroto for collecting additional material. We are also grateful to H. A. Britski, M. de Pinna, N. A. Menezes, O. Oyakawa, P. Pruvost, S. O. Kullander J. Snoeks, E. Vreven, and Z. Gabsi for the loan of material or/and hospitality during visits to their institutions; and to P. F. Amorim, A. Katz, and J.L.O. Mattos for their help with the image preparations and analyses.

Funding

This study was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico – Ministério de Ciência e Tecnologia), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), and PROTAX (Programa de Capacitação em Taxonomia). Collections were made with license number 32955–3, provided by ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Pedro H. N. Bragança.

Electronic supplementary material

ESM 1

(PDF 292 kb)

ESM 2

(XLS 20 kb)

ESM 3

(XLSX 16 kb)

ESM 4

(XLSX 9 kb)

ESM 5

(PDF 159 kb)

ESM 6

(PDF 164 kb)

ESM 7

(PDF 479 kb)

ESM 8

(PDF 251 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bragança, P.H.N., Costa, W.J.E.M. Time-calibrated molecular phylogeny reveals a Miocene–Pliocene diversification in the Amazon miniature killifish genus Fluviphylax (Cyprinodontiformes: Cyprinodontoidei). Org Divers Evol 18, 345–353 (2018). https://doi.org/10.1007/s13127-018-0373-7

Download citation

Keywords

  • Neotropical
  • Neogene
  • Paleodrainage
  • Pebas system
  • Amazon lampeye
  • Andean uplift