Abstract

In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation. Here we test these predictions of the viviparity driven conflict hypothesis (VDCH) in live-bearing poecilid fishes, a group showing multiple independent origins of placentation and extreme variation in male sexually selected traits. As predicted, male sexually selected traits are only gained in lineages that lack placentas; while there is little or no influence of male traits on the evolution of placentas. Both results are consistent with the mode of female provisioning governing the evolution of male attributes. Moreover, it is the presence of male sexually selected traits (pre-copulatory), rather than placentation (post-copulatory), that are associated with higher rates of speciation. These results highlight a causal interaction between female reproductive mode, male sexual selection and the rate of speciation, suggesting a role for conflict in shaping diverse aspects of organismal biology.

Highlights

  • In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation

  • Genomic conflict leaves an imprint on genomic architecture, mode of inheritance, and diverse features of organismal biology[1,2]

  • There is greater lability of male traits throughout the tree, which results in less certainty in defining the properties of the common ancestor of the subfamily

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Summary

Introduction

In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation. Both results are consistent with the mode of female provisioning governing the evolution of male attributes It is the presence of male sexually selected traits (pre-copulatory), rather than placentation (post-copulatory), that are associated with higher rates of speciation. There are diverse mechanisms of matrotrophy, one of which is placentotrophy, defined as the integration of specialized embryonic and maternal tissues into a placenta, which sustains and provisions developing young[6] This shift in provisioning embryos from before to after fertilization has evolved independently multiple times in most vertebrate classes[7] as well as in a diversity of invertebrate taxa[8]. The diverse and bewilderingly complex interactions between mother and embryo associated with placentas are hypothesized to be manifestations of this conflict[9]

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