Evolutionary biogeography of the freshwater fish family Anablepidae (Teleostei: Cyprinodontiformes), a marine-derived Neotropical lineage

Abstract

Cladistic biogeography is an evolutionary biogeographic approach that infers area relationships by comparing area cladograms derived from different phylogenetic hypotheses. The South American freshwater ichthyofauna is enriched by an extraordinary number of marine-derived lineages, presenting its own phylogenetic and biogeographic patterns. Here, we performed a Brooks Parsimony Analysis (BPA) with the latest phylogenetic proposals for Anablepidae to compare hypotheses about the historical relationships among areas previously recognized based on fish species from the Neotropical region. We found that the area relationships for Anablepidae are in accordance with the pattern evidenced for other marine-derived lineages. The general area cladogram obtained shows a three-area relationship pattern, where freshwater is the sister group of Pacific + Atlantic marine areas. Within the freshwater clade, Southern Brazil + Uruguay River basin and Northwestern Argentina + Midwestern Argentina form two clades. Vicariance, dispersal, and extinction events related to Miocene and Quaternary marine transgressions and ancient connections between the Iguaçu and Upper Uruguay River basins supported the historical relationships among areas proposed here. Our results may be applied to patterns shown by other marine-derived lineages, as well as other freshwater organisms not necessarily having marine origins.

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

Fig. 1
Fig. 2
Fig. 3

Data availability statement

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

References

  1. Abell, R., Thieme, M. L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S. C., Bussing, W., Stiassny, M. L. J., Skelton, P., Allen, G. R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J. V., Heibel, T. J., Wikramanayake, E., Olson, D., Lopez, H. L., Reis, R. E., Lundberg, J. G., Perez, M. H. S., & Petry, P. (2008). Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 58, 403–414.

    Google Scholar 

  2. Aguilera, G., Terán, G. E., Mirande, J. M., Alonso, F., Rometsch, S., Meyer, A., & Torres-Dowdall, J. (2019). Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family. PLoS One, 14, e0218810.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Amorim, P. F. (2018). Jenynsia lineata species complex, revision and new species description (Cyprinodontiformes: Anablepidae). Journal of Fish Biology, 92, 1312–1332.

    Google Scholar 

  4. Amorim, P. F., & Costa, W. J. E. M. (2018). Multigene phylogeny supports diversification of four-eyed fishes and one-sided live-bearers (Cyprinodontiformes: Anablepidae) related to major South American geological events. PLoS One, 13, e0199201.

    PubMed  PubMed Central  Google Scholar 

  5. Amorim, P. F., & Costa, W. J. E. M. (2019). Reconstructing biogeographic temporal events in the evolution of the livebearer fish genus Jenynsia based on total evidence analysis (Cyprinodontiformes: Anablepidae). Systematics and Biodiversity, 17, 124–133.

    Google Scholar 

  6. Angulo, R. J., Lessa, G. C., & Souza, M. C. (2006). A critical review of mid- to late-Holocene sea-level fluctuations on the eastern Brazilian coastline. Quaternary Science Reviews, 25, 486–506.

    Google Scholar 

  7. 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). Berkeley and Los Angeles: University of California Press.

    Google Scholar 

  8. Bloom, D. D., & Lovejoy, N. R. (2017). On the origins of marine-derived freshwater fishes in South America. Journal of Biogeography, 44, 1927–1938.

    Google Scholar 

  9. Bogan, S., Contreras, V. H., Agnolin, F., Tomassini, R. L., & Peralta, S. (2018). New genus and species of Anablepidae (Teleostei, Cyprinodontiformes) from the Late Miocene of Argentina. Journal of South American Earth Sciences, 88, 374–384.

    Google Scholar 

  10. Brea, M., & Zucol, A. F. (2011). The Paraná-Paraguay basin: geology and paleoenvironments. In J. S. Albert & R. E. Reis (Eds.), Historical biogeography of Neotropical freshwater fishes (pp. 69–88). Berkeley and Los Angeles: University of California Press.

    Google Scholar 

  11. Brooks, D. R. (1981). Hennig’s parasitological method: a proposed solution. Systematic Zoology, 30, 229–249.

    Google Scholar 

  12. Brooks, D. R. (1988). Macroevolutionary comparisons of host and parasite phylogenies. Annual Review of Ecology and Systematics, 19, 235–259.

    Google Scholar 

  13. Brooks, D. R. (1990). Parsimony analysis in historical biogeography and coevolution: methodological and theoretical update. Systematic Zoology, 39, 14–30.

    Google Scholar 

  14. Brooks, D. R., Thorson, T. B., & Mayes, M. A. (1981). Fresh-water stingrays (Potamotrygonidae) and their helminth parasites: testing hypotheses of evolution and coevolution. In V. A. Funk & D. R. Brooks (Eds.), Advances in cladistics (pp. 147–175). New York: New York Botanical Gardern.

    Google Scholar 

  15. Brooks, D. R., Van Veller, M. G. P., & McLennan, D. A. (2001). How to do BPA, really. Journal of Biogeography, 28, 345–358.

    Google Scholar 

  16. Bruno, M. C., Casciotta, J. R., Almirón, A. E., Ricillio, F. L., & Lizarrade, M. S. (2015). Quaternary refugia and secondary contact in the southern boundary of the Brazilian subregion: comparative phylogeography of freshwater fish. Vertebrate Zoology, 65, 45–55.

    Google Scholar 

  17. Calviño, P., & Alonso, F. (2016). First record of the genus Jenynsia from marine water on the coast of Punta del Este, Maldonado, Uruguay (Cyprinodontiformes: Anablepidae). Journal of Fish Biology, 88, 1236–1240.

    PubMed  Google Scholar 

  18. Cooke, G. M., Chao, N. L., & Beheregaray, L. B. (2012). Marine incursions, cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genus Plagioscion (Sciaenidae). Journal of Biogeography, 39, 724–738.

    Google Scholar 

  19. Costa, W. J. E. M. (2010). Historical biogeography of cynolebiasine annual killifishes inferred from dispersal-vicariance analysis. Journal of Biogeography, 37, 1995–2004.

    Google Scholar 

  20. Crisci, J. V., Katinas, L., & Posadas, P. (2003). Historical biogeography: an introduction. Cambridge: Harvard University Press.

    Google Scholar 

  21. da Silva, M., & Noll, F. B. (2015). Biogeography of the social wasp genus Brachygastra ( Hymenoptera: Vespidade: Polistinae). Journal of Biogeography, 42, 833–842.

    Google Scholar 

  22. de Carvalho, A. L. G., de Britto, M. R., & Fernandes, D. S. (2013). Biogeography of the lizard genus Tropidurus Wied-Neuwied, 1825 (Squamata: Tropiduridae): distribution, endemism, and area relationships in South America. PLoS One, 8, e59736.

    PubMed  PubMed Central  Google Scholar 

  23. Domning, D. P. (1982). Evolution of manatees: a speculative history. Journal of Paleontology, 56, 599–619.

    Google Scholar 

  24. 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.

    Google Scholar 

  25. Frota, A., Pavanelli, C. S., & da Graça, W. J. (2019). Areas of endemism for Anablepidae (Teleostei: Cyprinodontiformes): a monophyletic family of freshwater fishes in the Neotropics. Zootaxa, 4671, 527–540.

    Google Scholar 

  26. Goloboff, P., Farris, J. S., & Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.

    Google Scholar 

  27. Grabert, H. (1984). Migration and speciation of the South American Iniidae (Cetacea, Mammalia). Zeitschrift Fur Saugetierkunde-International Journal of Mammalian Biology, 49, 334–341.

    Google Scholar 

  28. Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T., Särkinen, T., & Antonelli, A. (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330, 927–931.

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  30. Hulka, C., Gräfe, K.-U., Sames, B., Uba, C. E., & Heubeck, C. (2006). Depositional setting of the Middle to Late Miocene Yecua Formation of the Chaco Foreland Basin, southern Bolivia. Journal of South American Earth Sciences, 21, 135–150.

    Google Scholar 

  31. Lovejoy, N. R. (1997). Stingrays, parasites, and Neotropical biogeography: a closer look at Brooks et al’s hypotheses concerning the origins of Neotropical freshwater rays (Potamotrygonidae). Systematic Biology, 46, 218–230.

    Google Scholar 

  32. Lovejoy, N. R., Bermingham, E., & Martin, A. P. (1998). Marine incursion into South America. Nature, 396, 421–422.

    CAS  Google Scholar 

  33. 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, 5–13.

    Google Scholar 

  34. Martin, L., Suguio, K., Flexor, J. M., Dominguez, J. M. L., & Bittencourt, A. C. S. P. (1996). Quaternary sea-level history and variation in dynamics along the Central Brazilian coast: consequences on coastal plain construction. Anais da Academia Brasileira de Ciências, 68, 303–354.

    Google Scholar 

  35. Morrone, J. J. (2005). Cladistic biogeography: identity and place. Journal of Biogeography, 32, 1281–1284.

    Google Scholar 

  36. Morrone, J. J. (2009). Evolutionary biogeoraphy: an integrative approach with case studies. New York: Columbia University Press.

    Google Scholar 

  37. Nihei, S. S. (2016). Biogeografia cladística. In C. J. Carvalho & E. A. B. Almeida (Eds.), Biogeografia da América do Sul: análise de tempo, espaço e forma (pp. 35–56) (2nd ed.). São Paulo: Roca.

    Google Scholar 

  38. Nixon, K. C. (2002). Winclada, Version 1.00.08. Published by the author.

  39. Nuttall, C. P. (1990). A review of the Tertiary non-marine molluscan faunas of the Pebasian and other inland basins of north-western South America. Bulletin of the British Museum of Natural History, Geology, 45, 165–371.

    Google Scholar 

  40. Parenti, L. R. (1981). A phylogenetic and biogeographic analysis of cyprinodontiform fishes (Teleostei, Atherinomorpha). Bulletin of the American Museum of Natural History, 168, 335–557.

    Google Scholar 

  41. Parenti, L. R., & Ebach, M. C. (2009). Comparative biogeography: discovering and classifying biogeographical patterns of a dynamic Earth. Berkeley and Los Angeles: University of California Press.

    Google Scholar 

  42. Pereira, T. L., Santos, U., Schaefer, C. E., Souza, G. O., Paiva, S. R., Malabarba, L. R., Schmidt, E. E., & Dergam, J. A. (2013). Dispersal and vicariance of Hoplias malabaricus (Bloch 1794) (Teleostei, Erythrinidae) populations of the Brazilian continental margin. Journal of Biogeography, 40, 905–914.

    Google Scholar 

  43. Platnick, N. I., & Nelson, G. (1978). A method of analysis for historical biogeography. Systematic Zoology, 27, 1–16.

    Google Scholar 

  44. Reis, R. E., Albert, J. S., Di Dario, F., Mincarone, M. M., Petry, P., & Rocha, L. A. (2016). Fish biodiversity and conservation in South America. Journal of Fish Biology, 89, 12–47.

    CAS  PubMed  Google Scholar 

  45. Ribeiro, A. C. (2006). Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotropical Ichthyology, 4, 225–246.

    Google Scholar 

  46. Rosen, D. E. (1978). Vicariant patterns and historical explanation in biogeography. Systematic Zoology, 27, 159–188.

    Google Scholar 

  47. Roxo, F. F., Albert, J. S., Silva, G. S. C., Zawadzki, C. H., Foresti, F., & Oliveira, C. (2014). Molecular phylogeny and biogeographic history of the armored Neotropical catfish subfamilies Hypoptopomatinae, Neoplecostominae and Otothyrinae (Siluriformes: Loricariidae). PLoS One, 9, e105564.

    PubMed  PubMed Central  Google Scholar 

  48. Sanmartín, I. (2007). Event-based biogeography: integrating patterns, processes, and time. In M. C. Ebach & R. S. Tangney (Eds.), Biogeography in a changing world (pp. 135–159). Boca Raton: CRC Press.

    Google Scholar 

  49. Sferco, E., Herbst, R., Aguilera, G., & Mirande, J. M. (2018). The rise of internal fertilization in the Anablepidae (Teleostei, Cyprinodontiformes): two new genera and species from the Miocene of Tucumán, Argentina. Papers in Palaeontology, 4, 177–195.

    Google Scholar 

  50. Thomaz, A. T., Malabarba, L. R., Bonatto, S. L., & Knowles, L. L. (2015). Testing the effect of palaeodrainages versus habitat stability on genetic divergence in Riverine systems: study of a Neotropical fish of the Brazilian coastal Atlantic forest. Journal of Biogeography, 42, 2389–2401.

    Google Scholar 

  51. Tschá, M. K., Bachmann, L., Abilhoa, V., & Boeger, W. A. (2017a). Past connection and isolation of catchments: the sea-level changes affect the distribution and genetic variability of coastal freshwater fishes. Estuarine, Coastal and Shelf Science, 190, 31–39.

    Google Scholar 

  52. Tschá, M. K., Baggio, R. A., Marteleto, F. M., Abilhoa, V., Bachmann, L., & Boeger, W. A. (2017b). Sea-level variations have influenced the demographic history of estuarine and freshwater fishes of the coastal plain of Paraná, Brazil. Journal of Fish Biology, 90, 968–979.

    PubMed  Google Scholar 

  53. Tumini, G., Giri, F., Williner, V., Collins, P. A., & Morrone, J. J. (2018). Distributional patterns of endemic southern South American freshwater aeglids (Crustacea: Decapoda: Anomura: Aeglidae). Zoologischer Anzeiger, 277, 55–64.

    Google Scholar 

  54. Van Veller, M. G. P., & Brooks, D. R. (2001). When simplicity is not parsimonious: a priori and a posteriori methods in historical biogeography. Journal of Biogeography, 28, 1–11.

    Google Scholar 

  55. Webb, S. D. (1995). Biological implications of the Middle Miocene Amazon seaway. Science, 269, 361–362.

    CAS  PubMed  Google Scholar 

  56. Wiley, E. O. (1988a). Parsimony analysis and vicariance biogeography. Systematic Zoology, 37, 271–290.

    Google Scholar 

  57. Wiley, E. O. (1988b). Vicariance biogeography. Annual Review of Ecology and Systematics, 19, 513–542.

    Google Scholar 

  58. Woodburne, M. O. (2010). The great American biotic interchange: dispersals, tectonics, climate, sea level and holding pens. Journal of Mammalian Evolution, 17, 245–264.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are deeply grateful to PEA (Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais) and Fundação Araucária (SETI/PR) for financial support given to A.F. for his research stay in Mexico. We thank CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for productivity scholarship conceived to W.J.G. (305200/2018-6) and postgraduation scholarship to A.F (141242/2018-3).

Funding

Fundação Araucária (SETI/PR) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), grants/award numbers: 141242/2018-3 and 305200/2018-6.

Author information

Affiliations

Authors

Contributions

A.F. conceived and designed the investigation; A.F. and J.J.M. performed the biogeographic analysis; J.J.M. and W.J.G. contributed to the data interpretation and critical revision for adding substantive intellectual content. All authors interpreted the data and wrote the manuscript.

Corresponding author

Correspondence to Augusto Frota.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not use animals and does not contain any studies with human participants performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Frota, A., Morrone, J.J. & da Graça, W.J. Evolutionary biogeography of the freshwater fish family Anablepidae (Teleostei: Cyprinodontiformes), a marine-derived Neotropical lineage. Org Divers Evol (2020). https://doi.org/10.1007/s13127-020-00444-1

Download citation

Keywords

  • Area cladogram
  • Components
  • Historical biogegraphy
  • Miocene
  • Neotropical region
  • Quaternary