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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.

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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.

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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.

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Correspondence to Kimberly A. Paczolt.

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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

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