The evolution of the placenta drives a shift in sexual selection in livebearing fish

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Abstract

The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent–offspring conflicts during pregnancy1,2,3,4. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection2. This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation5,6. We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.

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Figure 1: Phylogenetic tree showing relationships among 94 species of the fish family Poeciliidae.
Figure 2: Phylogenetic logistic and linear regressions.

Change history

  • 10 September 2014

    Author T.G. was added the author list; corresponding changes were made to the Acknowledgements and Author Contributions.

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Acknowledgements

We thank all individuals and institutions who provided samples for this study (Rehoboth Aquatics, H. Bart Jr, R. Davis, D. Fromm, J. de Greef, H. Hieronimus, B. Hobbs, T. Hrbek, J. Johnson, B. Kohler, J. Langenhammer, C. Li, J. Lundberg, M. Mateos, A. Meyer, D. Nelson, L. Page, L. Parenti, M. Sabaj Pérez, R. Robins, R. de Ruiter, S. Schaefer, M. Schartl, J. Sparks, M. Stiassny, J. Travis, J. Trexler and J. Williams); L. Rowe and A. Furness for discussions and reading the manuscript; and C. Oufiero and M. Banet for help in collecting part of the data. This study was supported by Rubicon grant 825.07.017 of the Netherlands Organisation for Scientific Research and Marie Curie – IIF grant 299048 of the European Union to B.J.A.P. and grant DEB0416085 of the US National Science Foundation to D.N.R. and M.S.S.

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Authors

Contributions

B.J.A.P. and D.N.R. designed the study, D.N.R. quantified the matrotrophy indices, R.W.M. and M.S.S. constructed the molecular phylogeny, T.G. taught B.J.A.P. how to do phylogenetic regression and aided in the preliminary analysis of the data, and B.J.A.P. measured the morphological traits, performed the final analyses of the data and wrote the paper. All authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to B. J. A. Pollux or D. N. Reznick.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Table 1 Results of models of molecular evolution chosen by jModelltest
Extended Data Table 2 Bayesian inference of correlated evolution between the natural-log-transformed matrotrophy index and other life-history traits within the family Poeciliidae
Extended Data Table 3 Bayesian inference of correlated evolution between the natural-log-transformed matrotrophy index and other life-history traits within the family Poeciliidae using a subset of ten trees to control for phylogenetic uncertainty
Extended Data Table 4 Bayesian inference of correlated evolution between the natural-log-transformed matrotrophy index and other life-history traits after data imputation with PhyloPars
Extended Data Table 5 Ordinary and phylogenetic logistic regression parameter estimates for the effect of the natural-log-transformed matrotrophy index on dichromatism, courtship behaviour, ornamental male display traits and superfetation within the family Poeciliidae
Extended Data Table 6 White’s general and Breusch–Pagan tests for homoscedasticity

Supplementary information

Supplementary Figure 1

This figure shows ML phylogram obtained with RAxML. (PDF 276 kb)

Supplementary Figure 2

This figure shows the maximum likelihood bootstrap support percentages. (PDF 355 kb)

Supplementary Tables

This file contains Supplementary Tables 1-6. (PDF 4544 kb)

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Pollux, B., Meredith, R., Springer, M. et al. The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature 513, 233–236 (2014). https://doi.org/10.1038/nature13451

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