Abstract

A live-bearing reproductive strategy can induce large morphological changes in the mother during pregnancy. The evolution of the placenta in swimming animals involves a shift in the timing of maternal provisioning from pre-fertilization (females supply their eggs with sufficient yolk reserves prior to fertilization) to post-fertilization (females provide all nutrients via a placenta during the pregnancy). It has been hypothesised that this shift, associated with the evolution of the placenta, should confer a morphological advantage to the females leading to a more slender body shape during the early stages of pregnancy. We tested this hypothesis by quantifying three-dimensional shape and volume changes during pregnancy and in full-grown virgin controls of two species within the live-bearing fish family Poeciliidae: Poeciliopsis gracilis (non-placental) and Poeciliopsis turneri (placental). We show that P. turneri is more slender than P. gracilis at the beginning of the interbrood interval and in virgins, and that these differences diminish towards the end of pregnancy. This study provides the first evidence for an adaptive morphological advantage of the placenta in live-bearing fish. A similar morphological benefit could drive the evolution of placentas in other live-bearing (swimming) animal lineages.

Highlights

  • IntroductionThe placenta, defined as an intimate apposition or fusion of maternal and foetal tissues for physiological exchange [1], has evolved many times independently throughout the animal kingdom (e.g. in invertebrates, fish, amphibians, reptiles and mammals; [2,3,4,5,6]), including at least eight times within the live-bearing fish family Poeciliidae [7,8,9,10]

  • The placenta, defined as an intimate apposition or fusion of maternal and foetal tissues for physiological exchange [1], has evolved many times independently throughout the animal kingdom, including at least eight times within the live-bearing fish family Poeciliidae [7,8,9,10]

  • We show that P. turneri is more slender than P. gracilis at the beginning of the interbrood interval and in virgins, and that these differences diminish towards the end of pregnancy

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Summary

Introduction

The placenta, defined as an intimate apposition or fusion of maternal and foetal tissues for physiological exchange [1], has evolved many times independently throughout the animal kingdom (e.g. in invertebrates, fish, amphibians, reptiles and mammals; [2,3,4,5,6]), including at least eight times within the live-bearing fish family Poeciliidae [7,8,9,10]. Despite the repeated emergence of placentas among widely diverged animal lineages, it is still unclear what selective forces drive the evolution of placental organs. Three non-mutually exclusive adaptive hypotheses have been proposed to explain why the placenta may have evolved in Poeciliid fish: the resource availability hypothesis, the life history facilitation hypothesis and the locomotor cost hypothesis. Effect of placenta evolution on pregnant fish morphology.

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