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

Abstract

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.

Change history

  • 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.

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Acknowledgements

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). https://doi.org/10.1038/s41559-017-0233-4

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