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


This article has been updated


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1

    Haig, D. Genetic conflicts in human pregnancy. Q. Rev. Biol. 68, 495–532 (1993)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Zeh, D. W. & Zeh, J. A. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. Bioessays 22, 938–946 (2000)

    Article  CAS  PubMed  Google Scholar 

  3. 3

    Wilkins, J. R. & Haig, D. What good is genomic imprinting: the function of parent-specific gene expression. Nature Rev. Genet. 4, 359–368 (2003)

    Article  CAS  PubMed  Google Scholar 

  4. 4

    Crespi, B. & Semeniuk, C. Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am. Nat. 163, 635–653 (2004)

    Article  PubMed  Google Scholar 

  5. 5

    Reznick, D. N., Mateos, M. & Springer, M. S. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298, 1018–1020 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  6. 6

    Pollux, B. J. A., Pires, M. N., Banet, A. I. & Reznick, D. N. The evolution of placentas in the fish family Poeciliidae – an empirical study of macroevolution. Annu. Rev. Ecol. Evol. Syst. 40, 271–289 (2009)

    Article  Google Scholar 

  7. 7

    Trivers, R. L. Parent-offspring conflict. Am. Zool. 14, 249–264 (1974)

    Article  Google Scholar 

  8. 8

    Banet, A. I., Au, A. G. & Reznick, D. N. Is mom in charge? Implications of resource provisioning on the evolution of the placenta. Evolution 64, 3172–3182 (2010)

    Article  PubMed  Google Scholar 

  9. 9

    Pollux, B. J. A. & Reznick, D. N. Matrotrophy limits a female’s ability to adaptively adjust offspring size and fecundity in fluctuating environments. Funct. Ecol. 25, 747–756 (2011)

    Article  Google Scholar 

  10. 10

    Zeh, J. A. & Zeh, D. W. Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109, 929–950 (2003)

    Article  Google Scholar 

  11. 11

    Haig, D. Brood reduction and optimal parental investment when offspring differ in quality. Am. Nat. 136, 550–556 (1990)

    Article  Google Scholar 

  12. 12

    Bisazza, A. Male competition, female mate choice and sexual size dimorphism in poeciliid fishes. Mar. Behav. Physiol. 23, 257–286 (1993)

    Article  Google Scholar 

  13. 13

    Meffe, G. K. & Snelson, F. F. Jr . (eds). Ecology and Evolution of Livebearing Fishes (Poeciliidae) (Prentice Hall, 1989)

    Google Scholar 

  14. 14

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

  15. 15

    Shackelford, R. M. Superfetation in the ranch mink. Am. Nat. 86, 311–319 (1952)

    Article  Google Scholar 

  16. 16

    Yamaguchi, N., Dugdale, H. L. & MacDonald, D. W. Female receptivity, embryonic diapause, and superfetation in the European badger (Meles meles): implications for the reproductive tactics of males and females. Q. Rev. Biol. 81, 34–48 (2006)

    Article  Google Scholar 

  17. 17

    Dugdale, H. L., MacDonald, D. W., Pope, L. C. & Burke, T. Polygynandry, extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups. Mol. Ecol. 16, 5294–5306 (2007)

    Article  PubMed  Google Scholar 

  18. 18

    O’Neill, M. J. et al. Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes. Proc. Natl Acad. Sci. USA 104, 12404–12409 (2007)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. 19

    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 

  20. 20

    Coleman, S. W., Harlin-Cognato, A. & Jones, A. G. Reproductive isolation, reproductive mode, and sexual selection: Empirical tests of the viviparity-driven conflict hypothesis. Am. Nat. 173, 291–303 (2009)

    Article  PubMed  Google Scholar 

  21. 21

    Schrader, M. & Travis, J. Variation in offspring size with birth order in placental fish: A role for asymmetric sibling competition? Evolution 66, 272–279 (2012)

    Article  PubMed  Google Scholar 

  22. 22

    Bisazza, A. & Marin, G. Sexual selection and sexual size dimorphism in the eastern mosquitofish Gambusia holbrooki (Pisces Poeciliidae). Ethol. Ecol. Evol. 7, 169–183 (1995)

    Article  Google Scholar 

  23. 23

    Pilastro, A., Giacomello, E. & Bisazza, A. Sexual selection for small size in male mosquitofish (Gambusia holbrooki). Proc. R. Soc. Lond. B 264, 1125–1129 (1997)

    Article  ADS  Google Scholar 

  24. 24

    Evans, J. P. et al. Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification. Proc. R. Soc. B 278, 2611–2620 (2011)

    Article  PubMed  Google Scholar 

  25. 25

    Arnqvist, G. & Rowe, L. Antagonistic coevolution between the sexes in a group of insects. Nature 415, 787–789 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  26. 26

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

    Article  PubMed  Google Scholar 

  27. 27

    Arnqvist, G. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784–786 (1998)

    Article  ADS  CAS  Google Scholar 

  28. 28

    Hosken, D. J. & Stockley, P. Sexual selection and genital evolution. Trends Ecol. Evol. 19, 88–93 (2004)

    Article  Google Scholar 

  29. 29

    Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006)

    Article  CAS  Google Scholar 

  30. 30

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

    Article  Google Scholar 

  31. 31

    Lovich, J. E. & Gibbons, J. W. A review of techniques for quantifying sexual size dimorphism. Growth Dev. Aging 56, 269–281 (1992)

    CAS  PubMed  Google Scholar 

  32. 32

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

  33. 33

    Meyer, A. & Lydeard, C. The evolution of copulatory organs, internal fertilization, placentae and viviparity in killifishes (Cyprinodontiformes) inferred from a DNA phylogeny of the tyrosine kinase gene X-src. Proc. R. Soc. Lond. B 254, 153–162 (1993)

    Article  ADS  CAS  Google Scholar 

  34. 34

    Meredith, R. W., Pires, M. N., Reznick, D. N. & Springer, M. S. Molecular phylogenetic relationships and the evolution of the placenta in Poecilia (Micropoecilia) (Poeciliidae: Cyprinodontiformes). Mol. Phylogenet. Evol. 55, 631–639 (2010)

    Article  PubMed  Google Scholar 

  35. 35

    Meredith, R. W., Pires, M. N., Reznick, D. N. & Springer, M. S. Molecular phylogenetic relationships and the coevolution of placentotrophy and superfetation in Poecilia (Poeciliidae: Cyprinodontiformes). Mol. Phylogenet. Evol. 59, 148–157 (2011)

    Article  PubMed  Google Scholar 

  36. 36

    Li, C., Ortí, G., Zhang, G. & Lu, G. A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 7, 44 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 37

    Chen, W. J., Bonillo, C. & Lecointre, G. Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol. Phylogenet. Evol. 26, 262–288 (2003)

    Article  CAS  PubMed  Google Scholar 

  38. 38

    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  CAS  PubMed  Google Scholar 

  39. 39

    Kocher, T. D., Conroy, J. A., McKaye, K. R., Stauffer, J. R. & Lockwood, S. F. Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Mol. Phylogenet. Evol. 4, 420–432 (1995)

    Article  CAS  PubMed  Google Scholar 

  40. 40

    Ptacek, M. B. & Breden, F. Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J. Fish Biol. 53 (Suppl. A). 64–81 (1998)

    Article  Google Scholar 

  41. 41

    Breden, F., Ptacek, M. B., Rashed, M., Taphorn, D. & Figueiredo, C. A. Molecular phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Mol. Phylogenet. Evol. 12, 95–104 (1999)

    Article  CAS  PubMed  Google Scholar 

  42. 42

    Schmidt, T. R., Bielawski, J. P. & Gold, J. R. Molecular phylogenetics and evolution of the cytochrome b gene in the cyprinid genus Lythrurus. Copeia 1998, 14–22 (1998)

    Article  Google Scholar 

  43. 43

    Rambaut, A. Se-Al: Sequence Alignment Editor v.2.0a11 (1996)

  44. 44

    Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

    Article  PubMed  Google Scholar 

  45. 45

    Posada, D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256 (2008)

    Article  CAS  PubMed  Google Scholar 

  46. 46

    Yang, Z. Computational Molecular Evolution (Oxford Univ. Press, 2006)

    Google Scholar 

  47. 47

    Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  48. 48

    Pagel, M. & Meade, A. User’s Manual for BayesTraits V2 (2013)

    Google Scholar 

  49. 49

    Bruggeman, J., Heringa, J. & Brandt, B. W. PhyloPars: estimation of missing parameter values using phylogeny. Nucleic Acids Res. 37, W179–W184 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Kass, R. E. & Raftery, A. E. Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995)

    Article  MathSciNet  MATH  Google Scholar 

  51. 51

    Ives, A. R. & Garland, T. Jr . Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9–26 (2010)

    Google Scholar 

  52. 52

    Maddison, W. P. & Maddison, D. R. Mesquite: A Modular System forEvolutionary Analysis v.2.75 (2011)

  53. 53

    Garland, T. Jr, Dickerman, A. W., Janis, C. M. & Jones, J. A. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42, 265–292 (1993)

    Article  Google Scholar 

  54. 54

    Lavin, S. R., Karasov, W. H., Ives, A. R., Middleton, K. M. & Garland, T. Jr . Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Physiol. Biochem. Zool. 81, 526–550 (2008)

    Article  PubMed  Google Scholar 

  55. 55

    SAS Institute SAS/ETS 12.1 User’s Guide 1121–1122 (SAS Institute, 2012)

    Google Scholar 

  56. 56

    Purvis, A. & Garland, T. Jr . Polytomies in comparative analyses of continuous characters. Syst. Biol. 42, 569–575 (1993)

    Article  Google Scholar 

  57. 57

    Garland, T. Jr & Díaz-Uriarte, R. Polytomies and phylogenetically independent contrasts: an examination of the bounded degrees of freedom approach. Syst. Biol. 48, 547–558 (1999)

    Article  PubMed  Google Scholar 

  58. 58

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn, 70–71 (Springer, 2002)

    Google Scholar 

  59. 59

    Felsenstein, J. Inferring Phylogenies (Sinauer, 2004)

    Google Scholar 

Download references


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.

Author information




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.

Ethics declarations

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)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing