Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy

Abstract

Male pregnancy in seahorses, pipefishes and sea dragons (family Syngnathidae) represents a striking reproductive adaptation that has shaped the evolution of behaviour and morphology in this group of fishes1,2,3,4. In many syngnathid species, males brood their offspring in a specialized pouch, which presumably evolved to facilitate male parental care5,6. However, an unexplored possibility is that brood pouch evolution was partly shaped by parent–offspring or sexual conflict, processes that would result in trade-offs between current and future pregnancies. Here we report a controlled breeding experiment using the sexually dimorphic Gulf pipefish, Syngnathus scovelli, to test for post-copulatory sexual selection within broods and for trade-offs between successive male pregnancies as functions of female attractiveness. Offspring survivorship within a pregnancy was affected by the size of a male’s mate, the number of eggs transferred and the male’s sexual responsiveness. Significantly, we also found that embryo survivorship in a current pregnancy was negatively related to survivorship in the prior pregnancy, clearly demonstrating fitness trade-offs between broods. Overall, our data indicate that post-copulatory sexual selection and sexual conflict occur in Gulf pipefishes. The conflict seems to be mediated by a strategy of cryptic choice in which males increase rates of offspring abortion in pregnancies from unattractive mothers to retain resources for future reproductive opportunities. Hence, the male brood pouch of syngnathid fishes, which nurtures offspring7,8,9, also seems to have an important role as an arbiter of conflict between the sexes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Experimental design and brood pouch morphology.
Figure 2: Evidence for pre-copulatory mate choice and post-copulatory sexual selection by male Gulf pipefishes.
Figure 3: Results of a path analysis showing the effects of variables from the prior and current broods on current offspring survivorship.

Similar content being viewed by others

References

  1. Berglund, A., Rosenqvist, G. & Svensson, I. Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav. Ecol. Sociobiol. 19, 301–307 (1986)

    Article  Google Scholar 

  2. Vincent, A., Ahnesjö, I., Berglund, A. & Rosenqvist, G. Pipefishes and seahorses–are they all sex-role reversed? Trends Ecol. Evol. 7, 237–241 (1992)

    Article  CAS  Google Scholar 

  3. Jones, A. G., Rosenqvist, G., Berglund, A., Arnold, S. J. & Avise, J. C. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proc. R. Soc. Lond. B 267, 677–680 (2000)

    Article  CAS  Google Scholar 

  4. Wilson, A. B., Ahnesjö, I., Vincent, A. C. J. & Meyer, A. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae). Evolution 57, 1374–1386 (2003)

    Article  Google Scholar 

  5. Harlin-Cognato, A., Hoffman, E. A. & Jones, A. G. Gene co-option without duplication during the evolution of a male pregnancy gene in pipefish. Proc. Natl Acad. Sci. USA 103, 19407–19412 (2006)

    Article  ADS  CAS  Google Scholar 

  6. Stölting, K. N. & Wilson, A. B. Male pregnancy in seahorses and pipefish: beyond the mammalian model. Bioessays 29, 884–896 (2007)

    Article  Google Scholar 

  7. Berglund, A., Rosenqvist, G. & Svensson, I. Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species. Mar. Ecol. Prog. Ser. 29, 209–215 (1986)

    Article  ADS  Google Scholar 

  8. Ripley, J. L. & Foran, C. M. Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). J. Exp. Biol. 209, 1112–1121 (2006)

    Article  Google Scholar 

  9. Ripley, J. L. & Foran, C. M. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). J. Comp. Physiol. B 179, 325–333 (2009)

    Article  Google Scholar 

  10. Dawson, C. E. Indo-Pacific Pipefishes (Gulf Coast Research Lab, 1985)

    Google Scholar 

  11. Herald, E. S. From pipefish to seahorse–a study of phylogenetic relationships. Proc. Calif. Acad. Sci. 29, 465–473 (1959)

    Google Scholar 

  12. Partridge, C., Shardo, J. & Boettcher, A. Osmoregulatory role of the brood pouch in the euryhaline Gulf pipefish, Syngnathus scovelli. Comp. Biochem. Physiol. A 147, 556–561 (2007)

    Article  Google Scholar 

  13. Ripley, J. L. Osmoregulatory role of the paternal brood pouch for two Syngnathus species. Comp. Biochem. Physiol. A 154, 98–104 (2009)

    Article  Google Scholar 

  14. Berglund, A. & Rosenqvist, G. Sex role reversal in pipefish. Adv. Stud. Behav. 32, 131–167 (2003)

    Article  Google Scholar 

  15. Sagebakken, G., Ahnesjö, I., Mobley, K. B., Braga Gonçalves, I. & Kvarnemo, C. Brooding fathers, not siblings, take up nutrients from embryos. Proc. R. Soc. Lond. B 10.1098/rspb.2009.1767

  16. Trivers, R. L. in Sexual Selection and the Descent of Man (ed. Campbell, B.) 136–179 (Aldine, 1972)

    Google Scholar 

  17. Parker, G. A., Royle, N. J. & Hartley, I. R. Intrafamilial conflict and parental investment: a synthesis. Phil. Trans. R. Soc. Lond. B 357, 295–307 (2002)

    Article  Google Scholar 

  18. Arnqvist, G. & Rowe, L. Sexual Conflict (Princeton Univ. Press, 2005)

    Book  Google Scholar 

  19. Burley, N. The differential allocation hypothesis–an experimental test. Am. Nat. 132, 611–628 (1988)

    Article  Google Scholar 

  20. Sheldon, B. C. Differential allocation: tests, mechanisms and implications. Trends Ecol. Evol. 15, 397–402 (2000)

    Article  CAS  Google Scholar 

  21. Wolfner, M. F. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85–93 (2002)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Jones, A. G., Walker, D. & Avise, J. C. Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish. Proc. R. Soc. Lond. B 268, 2531–2535 (2001)

    Article  CAS  Google Scholar 

  24. Jones, A. G. & Avise, J. C. Microsatellite analysis of maternity and the mating system in the Gulf pipefish Syngnathus scovelli, a species with male pregnancy and sex-role reversal. Mol. Ecol. 6, 203–213 (1997)

    Article  CAS  Google Scholar 

  25. Ahnesjö, I. Apparent resource competition among embryos in the brood pouch of a male pipefish. Behav. Ecol. Sociobiol. 38, 167–172 (1996)

    Article  Google Scholar 

  26. Partridge, C. et al. The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish. Behav. Ecol. Sociobiol. 63, 345–354 (2009)

    Article  Google Scholar 

  27. Andersson, M. & Simmons, L. W. Sexual selection and mate choice. Trends Ecol. Evol. 21, 296–302 (2006)

    Article  Google Scholar 

  28. Hunt, J., Breuker, C. J., Sadowski, J. A. & Moore, A. J. Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22, 13–26 (2009)

    Article  Google Scholar 

  29. Scobell, S. K., Fudickar, A. M. & Knapp, R. Potential reproductive rate of a sex-role reversed pipefish over several bouts of mating. Anim. Behav. 78, 747–753 (2009)

    Article  Google Scholar 

  30. Brown, J. D. A Comparative Life History Study of Four Species of Pipefishes (Family Syngnathidae) in Florida. PhD thesis, Univ. Florida (1972)

    Google Scholar 

  31. Steiger, J. H. & Lind, J. C. Statistically based tests for the number of common factors. Proc. Ann. Spring Meeting Psychometric Soc. (1980)

Download references

Acknowledgements

This work was supported by grant IOS-0455927 from the US National Science Foundation. We thank S. Scobell and R. Carter for help with animal husbandry. We are also grateful to S. Arnold, A. Berglund, M. Giresi, N. Ratterman, E. Rose, G. Rosenthal, C. Small and D. Zeh for comments on the manuscript.

Author Contributions K.A.P. performed the experiments. A.G.J. and K.A.P. designed the experiments, analysed the data and wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kimberly A. Paczolt.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Analysis, Supplementary References and Supplementary Figures S1-S4 with legends. (PDF 394 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paczolt, K., Jones, A. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464, 401–404 (2010). https://doi.org/10.1038/nature08861

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08861

This article is cited by

Comments

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.

Search

Quick links

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