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Sex-specific evolution during the diversification of live-bearing fishes

A Publisher Correction to this article was published on 30 August 2018

This article has been updated


Natural selection is often assumed to drive parallel functional diversification of the sexes. But males and females exhibit fundamental differences in their biology, and it remains largely unknown how sex differences affect macroevolutionary patterns. On microevolutionary scales, we understand how natural and sexual selection interact to give rise to sex-specific evolution during phenotypic diversification and speciation. Here we show that ignoring sex-specific patterns of functional trait evolution misrepresents the macroevolutionary adaptive landscape and evolutionary rates for 112 species of live-bearing fishes (Poeciliidae). Males and females of the same species evolve in different adaptive landscapes. Major axes of female morphology were correlated with environmental variables but not reproductive investment, while male morphological variation was primarily associated with sexual selection. Despite the importance of both natural and sexual selection in shaping sex-specific phenotypic diversification, species diversification was overwhelmingly associated with ecological divergence. Hence, the inter-predictability of mechanisms of phenotypic and species diversification may be limited in many systems. These results underscore the importance of explicitly addressing sex-specific diversification in empirical and theoretical frameworks of evolutionary radiations to elucidate the roles of different sources of selection and constraint.

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Figure 1: Results of adaptive landscape analyses for male, female and sex-averaged body shape data using the best scoring tree.
Figure 2: Relative contributions of different mechanisms on species diversification.

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  • 30 August 2018

    In the version of this Article originally published, some production notes starting “Should we change...” were mistakenly left in at the end of the section ‘Sexual selection’; these notes have now been removed.


  1. 1.

    Wainwright, P. C. & Reilly, S. M. Ecological Morphology: Integrative Organismal Biology (Univ. Chicago Press, Chicago 1994).

    Google Scholar 

  2. 2.

    Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, New York, 1944).

    Google Scholar 

  3. 3.

    Nosil, P. Ecological Speciation (Oxford Univ. Press, Oxford, 2012).

    Book  Google Scholar 

  4. 4.

    Osborn, H. F. The law of adaptive radiation. Am. Nat. 36, 353–363 (1902).

    Article  Google Scholar 

  5. 5.

    Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000).

    Google Scholar 

  6. 6.

    Bateman, A. lntra-sexual selection in Drosophila. Heredity 2, 349–368 (1948).

    Article  PubMed  CAS  Google Scholar 

  7. 7.

    Andersson, M. B. Sexual Selection (Princeton Univ. Press, Princeton, 1994).

  8. 8.

    Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981).

    Article  PubMed  CAS  Google Scholar 

  9. 9.

    Boggs, C. L. Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecol. Entomol. 11, 7–15 (1986).

    Article  Google Scholar 

  10. 10.

    Queller, D. C. Why do females care more than males? Proc. R. Soc. Lond. B 264, 1555–1557 (1997).

    Article  Google Scholar 

  11. 11.

    Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009).

    Article  PubMed  Google Scholar 

  12. 12.

    Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (Oxford Univ. Press, Oxford, 2007).

    Book  Google Scholar 

  13. 13.

    Safran, R. J., Scordato, E. S. C., Symes, L. B., Rodríguez, R. L. & Mendelson, T. C. Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda. Trends Ecol. Evol. 28, 643–650 (2013).

    Article  PubMed  Google Scholar 

  14. 14.

    Reding, L., Swaddle, J. & Murphy, H. Sexual selection hinders adaptation in experimental populations of yeast. Biol. Lett. 9, 20121202 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. 15.

    Chenoweth, S. F., Appleton, N. C., Allen, S. L. & Rundle, H. D. Genomic evidence that sexual selection impedes adaptation to a novel environment. Curr. Biol. 25, 1860–1866 (2015).

    Article  PubMed  CAS  Google Scholar 

  16. 16.

    Butler, M. A., Sawyer, S. A. & Losos, J. B. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447, 202–205 (2007).

    Article  PubMed  CAS  Google Scholar 

  17. 17.

    Pincheira-Donoso, D., Hodgson, D. J., Stipala, J. & Tregenza, T. A phylogenetic analysis of sex-specific evolution of ecological morphology in Liolaemus lizards. Ecol. Res. 24, 1223–1231 (2009).

    Article  Google Scholar 

  18. 18.

    Lindenfors, P., Revell, L. J. & Nunn, C. L. Sexual dimorphism in primate aerobic capacity: a phylogenetic test. J. Evol. Biol. 23, 1183–1194 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Da Silva, J. M., Herrel, A., Measey, G. J. & Tolley, K. A. Sexual dimorphism in bite performance drives morphological variation in chameleons. PLoS ONE 9, e86846 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. 20.

    Pollux, B., Pires, M., Banet, A. & Reznick, D. Evolution of placentas in the fish family Poeciliidae: an empirical study of macroevolution. Ann. Rev. Ecol. Evol. Syst. 40, 271–289 (2009).

    Article  Google Scholar 

  21. 21.

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

    Article  PubMed  CAS  Google Scholar 

  22. 22.

    Evans, J. P., Pilastro, A. & Schlupp, I. Ecology and Evolution of Poeciliid Fishes (Univ. Chicago Press, Chicago, 2011).

    Book  Google Scholar 

  23. 23.

    Langerhans, R. B. & Reznick, D. N. in Fish Locomotion: An Etho-Ecological Perspective (eds Domenici, P. & Kapoor, B. G.) 200–248 (CRC, Cornell, 2010).

  24. 24.

    MacLaren, R. D., Gagnon, J. & He, R. Female bias for enlarged male body and dorsal fins in Xiphophorus variatus. Behav. Process. 87, 197–202 (2011).

    Article  Google Scholar 

  25. 25.

    Greenway, R., Drexler, S., Arias‐Rodriguez, L. & Tobler, M. Adaptive, but not condition‐dependent, body shape differences contribute to assortative mating preferences during ecological speciation. Evolution 70, 2809–2822 (2016).

    Article  PubMed  Google Scholar 

  26. 26.

    Rios-Cardenas, O. & Morris, M. R. in Ecology and Evolution of Poeciliid Fishes (eds Evans, J. P. et al.) 187–196 (Univ. Chicago Press, Chicago, 2011).

  27. 27.

    Ghalambor, C. K., Reznick, D. N. & Walker, J. A. Constraints on adaptive evolution: the functional trade‐off between reproduction and fast‐start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am. Nat. 164, 38–50 (2004).

    Article  PubMed  Google Scholar 

  28. 28.

    Zúñiga‐Vega, J., Suárez‐Rodríguez, M., Espinosa‐Pérez, H. & Johnson, J. Morphological and reproductive variation among populations of the Pacific molly Poecilia butleri. J. Fish Biol. 79, 1029–1046 (2011).

    Article  PubMed  Google Scholar 

  29. 29.

    Ciccotto, P. J. & Mendelson, T. C. The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae). Evolution 70, 745–756 (2016).

    Article  PubMed  Google Scholar 

  30. 30.

    Frías-Alvarez, P., Garcia, C. M., Vázquez-Vega, L. F. & Zúñiga-Vega, J. J. Spatial and temporal variation in superfoetation and related life history traits of two viviparous fishes: Poeciliopsis gracilis and P. infans. Naturwissenschaften 101, 1085–1098 (2014).

    Article  PubMed  CAS  Google Scholar 

  31. 31.

    Langerhans, R. B. Trade‐off between steady and unsteady swimming underlies predator‐driven divergence in Gambusia affinis. J. Evol. Biol. 22, 1057–1075 (2009).

    Article  PubMed  CAS  Google Scholar 

  32. 32.

    Rosenthal, G. G. & Garcia de Leon, F. J. in Ecology and Evolution of Poeciliid Fishes (eds Evans, J. P. et al.) 109–119 (Univ. Chicago Press, Chicago, 2011).

  33. 33.

    Zeh, J. A. & Zeh, D. W. Viviparity‐driven conflict: more to speciation than meets the fly. Ann. N. Y. Acad. Sci. 1133, 126–148 (2008).

    Article  PubMed  CAS  Google Scholar 

  34. 34.

    Langerhans, R. B., Gifford, M. E. & Joseph, E. O. Ecological speciation in Gambusia fishes. Evolution 61, 2056–2074 (2007).

    Article  PubMed  CAS  Google Scholar 

  35. 35.

    Plath, M. et al. Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments. Evolution 67, 2647–2661 (2013).

    Article  PubMed  Google Scholar 

  36. 36.

    Ingley, S. J. & Johnson, J. B. Divergent natural selection promotes immigrant inviability at early and late stages of evolutionary divergence. Evolution 70, 600–616 (2016).

    Article  PubMed  Google Scholar 

  37. 37.

    Rabosky, D. L. et al. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat. Commun. 4, 1958 (2013).

    Article  PubMed  CAS  Google Scholar 

  38. 38.

    Blom, M. P., Horner, P. & Moritz, C. Convergence across a continent: adaptive diversification in a recent radiation of Australian lizards. Proc. R. Soc. B 283, 20160181 (2016).

    Article  PubMed  Google Scholar 

  39. 39.

    Wagner, C. E., Harmon, L. J. & Seehausen, O. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487, 366–369 (2012).

    Article  PubMed  CAS  Google Scholar 

  40. 40.

    Arnegard, M. E. et al. Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am. Nat. 176, 335–356 (2010).

    Article  PubMed  Google Scholar 

  41. 41.

    Winger, B. M. & Bates, J. M. The tempo of trait divergence in geographic isolation: avian speciation across the Marañon Valley of Peru. Evolution 69, 772–787 (2015).

    Article  PubMed  Google Scholar 

  42. 42.

    Rabosky, D. L. & Matute, D. R. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proc. Natl Acad. Sci. USA 110, 15354–15359 (2013).

    Article  PubMed  Google Scholar 

  43. 43.

    Schrader, M. & Travis, J. Testing the viviparity‐driven‐conflict hypothesis: parent–offspring conflict and the evolution of reproductive isolation in a poeciliid fish. Am. Nat. 172, 806–817 (2008).

    Article  PubMed  Google Scholar 

  44. 44.

    Qualls, C. P. & Shine, R. Maternal body-volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity. Oecologia 103, 73–78 (1995).

    Article  PubMed  Google Scholar 

  45. 45.

    Pyron, R. A. & Burbrink, F. T. Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol. Lett. 17, 13–21 (2014).

    Article  PubMed  Google Scholar 

  46. 46.

    Helmstetter, A. J. et al. Viviparity stimulates diversification in an order of fish. Nat. Commun. 7, 11271 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. 47.

    Aristide, L. et al. Brain shape convergence in the adaptive radiation of New World monkeys. Proc. Natl Acad. Sci. USA 113, 2158–2163 (2016).

    Article  PubMed  CAS  Google Scholar 

  48. 48.

    Adams, D. C., Berns, C. M., Kozak, K. H. & Wiens, J. J. Are rates of species diversification correlated with rates of morphological evolution? Proc. R. Soc. B 276, 2729–2738 (2009).

    Article  PubMed  Google Scholar 

  49. 49.

    Salariato, D. L. & Zuloaga, F. O. Climatic niche evolution in the Andean genus Menonvillea (Cremolobeae: Brassicaceae). Org. Divers. Evol. 17, 11–28 (2017).

    Article  Google Scholar 

  50. 50.

    Rohlf, F. tpsDig (State University of New York, New York, 2004);

  51. 51.

    Zelditch, M., Swiderski, D., Sheets, H. & Fink, W. Geometric Morphometrics for Biologists (Elsevier Academic, 2004).

    Google Scholar 

  52. 52.

    Rohlf, F. tpsRelw (State University of New York, New York, 2007);

  53. 53.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Google Scholar 

  54. 54.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. 55.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. 56.

    Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article  PubMed  CAS  Google Scholar 

  57. 57.

    Vaidya, G., Lohman, D. J. & Meier, R. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180 (2011).

    Article  Google Scholar 

  58. 58.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. 59.

    Hrbek, T., Seckinger, J. & Meyer, A. A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Mol. Phylogenet. Evol. 43, 986–998 (2007).

    Article  PubMed  CAS  Google Scholar 

  60. 60.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  PubMed  CAS  Google Scholar 

  61. 61.

    Ho, A. L., Pruett, C. L. & Lin, J. Phylogeny and biogeography of Poecilia (Cyprinodontiformes: Poeciliinae) across Central and South America based on mitochondrial and nuclear DNA markers. Mol. Phylogenet. Evol. 101, 32–45 (2016).

    Article  PubMed  Google Scholar 

  62. 62.

    Santini, F., Harmon, L. J., Carnevale, G. & Alfaro, M. E. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol. Biol. 9, 194 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. 63.

    West, R. C. in Handbook of Middle American Indians (eds Wauchop, R. & West, R. C.) 33–83 (Univ. Texas Press, Austin, 1964).

  64. 64.

    Mateos, M., Sanjur, O. I. & Vrijenhoek, R. C. Historical biogeography of the livebearing fish genus Poeciliopsis (Poeciliidae: Cyprinodontiformes). Evolution 56, 972–984 (2002).

    Article  PubMed  Google Scholar 

  65. 65.

    Adams, D. C. Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Syst. Biol. 63, 166–177 (2013).

    Article  PubMed  Google Scholar 

  66. 66.

    van Proosdij, A. S., Sosef, M. S., Wieringa, J. J. & Raes, N. Minimum required number of specimen records to develop accurate species distribution models. Ecography 39, 542–552 (2015).

    Article  Google Scholar 

  67. 67.

    Miller, R. R., Minckley, W. L., Norris, S. M. & Gach, M. H. Freshwater Fishes of Mexico (Univ. Chicago Press, Chicago, 2005).

  68. 68.

    Bussing, W. A. Peces de las Aguas Continentales de Costa Rica - Freshwater Fishes of Costa Rica (Editorial de la Universidad de Costa Rica, San Jose, 1998).

    Google Scholar 

  69. 69.

    Sexton, J. P., McIntyre, P. J., Angert, A. L. & Rice, K. J. Evolution and ecology of species range limits. Ann. Rev. Ecol. Evol. Syst. 40, 415–436 (2009).

    Article  Google Scholar 

  70. 70.

    Jackson, D. A. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74, 2204–2214 (1993).

    Article  Google Scholar 

  71. 71.

    Kahn, A. T., Mautz, B. & Jennions, M. D. Females prefer to associate with males with longer intromittent organs in mosquitofish. Biol. Lett. 6, 55–58 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    MacLaren, R. D., Rowland, W. J. & Morgan, N. Female preferences for sailfin and body size in the sailfin molly, Poecilia latipinna. Ethology 110, 363–379 (2004).

    Article  Google Scholar 

  73. 73.

    Olivera‐Tlahuel, C., Ossip‐Klein, A. G., Espinosa‐Pérez, H. S. & Zúñiga‐Vega, J. J. Have superfetation and matrotrophy facilitated the evolution of larger offspring in poeciliid fishes? Biol. J. Linn. Soc. 116, 787–804 (2015).

    Article  Google Scholar 

  74. 74.

    Ingram, T. & Mahler, D. L. SURFACE: detecting convergent evolution from comparative data by fitting Ornstein–Uhlenbeck models with stepwise Akaike information criterion. Methods Ecol. Evol. 4, 416–425 (2013).

    Article  Google Scholar 

  75. 75.

    Khabbazian, M., Kriebel, R., Rohe, K. & Ané, C. Fast and accurate detection of evolutionary shifts in Ornstein–Uhlenbeck models. Methods Ecol. Evol. 7, 811–824 (2016).

    Article  Google Scholar 

  76. 76.

    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Development Core Team nlme: linear and nonlinear mixed effects models. R package version 3.1-103 (R Foundation for Statistical Computing, Vienna, 2013).

  77. 77.

    Martin, M. D. & Mendelson, T. C. The accumulation of reproductive isolation in early stages of divergence supports a role for sexual selection. J. Evol. Biol. 29, 676–689 (2016).

    Article  PubMed  CAS  Google Scholar 

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We thank the federal and local governments of Mexico and Costa Rica for permission to conduct research. The University of Michigan Museum of Zoology Fish Collection, especially collection manager D. Nelson, provided access and space to examine specimens. We are also indebted to the Academy of Natural Sciences of Philadelphia (M. Sabaj Pérez) and the Florida Museum of Natural History Division of Ichthyology (R. Robins) for providing access to additional specimens. In addition, we thank G. Alcaraz (UNAM), M. Cummings (Univ. Texas) and M. Ryan (Univ. Texas) for providing photos of specimens, and R. Safran and D. Reznick for providing helpful comments that improved the manuscript. J. Valvo kindly supplied the picture of M. picta and I. Tavares of A. reticulatus for Fig. 2. Finally, we thank C. E. Bautista-Hernandez for help in photographing specimens. Financial support was provided by an American Philosophical Society Franklin Research Grant to Z.W.C. and by the National Science Foundation (IOS-1463720 and IOS-1557860) to M.T.

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Z.W.C. and M.T. conceived the project. Z.W.C. collected and analysed the data. Z.W.C. and M.T. wrote the manuscript.

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Correspondence to Zachary W. Culumber or Michael Tobler.

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Culumber, Z.W., Tobler, M. Sex-specific evolution during the diversification of live-bearing fishes. Nat Ecol Evol 1, 1185–1191 (2017).

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