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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Wainwright, P. C. & Reilly, S. M. Ecological Morphology: Integrative Organismal Biology (Univ. Chicago Press, Chicago 1994).
Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, New York, 1944).
Nosil, P. Ecological Speciation (Oxford Univ. Press, Oxford, 2012).
Osborn, H. F. The law of adaptive radiation. Am. Nat. 36, 353–363 (1902).
Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000).
Bateman, A. lntra-sexual selection in Drosophila. Heredity 2, 349–368 (1948).
Andersson, M. B. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981).
Boggs, C. L. Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecol. Entomol. 11, 7–15 (1986).
Queller, D. C. Why do females care more than males? Proc. R. Soc. Lond. B 264, 1555–1557 (1997).
Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009).
Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (Oxford Univ. Press, Oxford, 2007).
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).
Reding, L., Swaddle, J. & Murphy, H. Sexual selection hinders adaptation in experimental populations of yeast. Biol. Lett. 9, 20121202 (2013).
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).
Butler, M. A., Sawyer, S. A. & Losos, J. B. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447, 202–205 (2007).
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).
Lindenfors, P., Revell, L. J. & Nunn, C. L. Sexual dimorphism in primate aerobic capacity: a phylogenetic test. J. Evol. Biol. 23, 1183–1194 (2010).
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).
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).
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).
Evans, J. P., Pilastro, A. & Schlupp, I. Ecology and Evolution of Poeciliid Fishes (Univ. Chicago Press, Chicago, 2011).
Langerhans, R. B. & Reznick, D. N. in Fish Locomotion: An Etho-Ecological Perspective (eds Domenici, P. & Kapoor, B. G.) 200–248 (CRC, Cornell, 2010).
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).
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).
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).
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).
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).
Ciccotto, P. J. & Mendelson, T. C. The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae). Evolution 70, 745–756 (2016).
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).
Langerhans, R. B. Trade‐off between steady and unsteady swimming underlies predator‐driven divergence in Gambusia affinis. J. Evol. Biol. 22, 1057–1075 (2009).
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).
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).
Langerhans, R. B., Gifford, M. E. & Joseph, E. O. Ecological speciation in Gambusia fishes. Evolution 61, 2056–2074 (2007).
Plath, M. et al. Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments. Evolution 67, 2647–2661 (2013).
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).
Rabosky, D. L. et al. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat. Commun. 4, 1958 (2013).
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).
Wagner, C. E., Harmon, L. J. & Seehausen, O. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487, 366–369 (2012).
Arnegard, M. E. et al. Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am. Nat. 176, 335–356 (2010).
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).
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).
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).
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).
Pyron, R. A. & Burbrink, F. T. Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol. Lett. 17, 13–21 (2014).
Helmstetter, A. J. et al. Viviparity stimulates diversification in an order of fish. Nat. Commun. 7, 11271 (2016).
Aristide, L. et al. Brain shape convergence in the adaptive radiation of New World monkeys. Proc. Natl Acad. Sci. USA 113, 2158–2163 (2016).
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).
Salariato, D. L. & Zuloaga, F. O. Climatic niche evolution in the Andean genus Menonvillea (Cremolobeae: Brassicaceae). Org. Divers. Evol. 17, 11–28 (2017).
Rohlf, F. tpsDig (State University of New York, New York, 2004); http://life.bio.sunysb.edu/morph/
Zelditch, M., Swiderski, D., Sheets, H. & Fink, W. Geometric Morphometrics for Biologists (Elsevier Academic, 2004).
Rohlf, F. tpsRelw (State University of New York, New York, 2007); http://life.bio.sunysb.edu/morph/
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
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).
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
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).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Hrbek, T., Seckinger, J. & Meyer, A. A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Mol. Phylogenet. Evol. 43, 986–998 (2007).
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
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).
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).
West, R. C. in Handbook of Middle American Indians (eds Wauchop, R. & West, R. C.) 33–83 (Univ. Texas Press, Austin, 1964).
Mateos, M., Sanjur, O. I. & Vrijenhoek, R. C. Historical biogeography of the livebearing fish genus Poeciliopsis (Poeciliidae: Cyprinodontiformes). Evolution 56, 972–984 (2002).
Adams, D. C. Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Syst. Biol. 63, 166–177 (2013).
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).
Miller, R. R., Minckley, W. L., Norris, S. M. & Gach, M. H. Freshwater Fishes of Mexico (Univ. Chicago Press, Chicago, 2005).
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).
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).
Jackson, D. A. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74, 2204–2214 (1993).
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).
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).
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).
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).
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).
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).
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).
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.
The authors declare no competing financial interests.
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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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