Why do placentas evolve? Evidence for a morphological advantage during pregnancy in live-bearing fish

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.

Maternal size and body condition predict the amount of post‐fertilization maternal provisioning in matrotrophic fish

“…In mammals, fetal fat deposition during pregnancy is however relatively insignificant (Elphick, Hull, & Broughton Pipkin, ), since most lipids are allocated to offspring postnatally, that is, during lactation (Bell, ). One might argue that the late (in fish) or relatively insignificant (in mammals) allocation of fat during pregnancy could be an adaptive feature of mobile matrotrophic live‐bearing animals in general, because studies have shown that an increase in reproductive allocation (i.e., the proportion of the mother's mass allocated to developing offspring) during pregnancy can lead to a less slender body shape (Fleuren, Quicazan‐Rubio, van Leeuwen, & Pollux, ) and negatively affect female locomotor performance in a wide range of viviparous taxa (e.g., fish, Plaut, ; Reznick, Bryant, Roff, Ghalambor, & Chalambor, ; reptiles, Seigel, Huggins, & Ford, ; and mammals, Noren, Redfern, & Edwards, ), which consequently may reduce survival probability (Laidlaw, Condon, & Belk, ; Plath, Riesch, Culumber, Streit, & Tobler, ). Thus, we suggest that the late allocation of fat might be adaptive, because earlier allocation of resources would unnecessarily increase the reproductive burden suffered by a pregnant female, and negatively impact her locomotor performance and, hence, her chance of survival.…”

Predation risk shapes the degree of placentation in natural populations of live‐bearing fish

“…A number of recent studies seem to support this idea. Fleuren et al (2018) showed that placental species are more slender at the beginning of pregnancy compared to non‐placental ones and that, consistent with the locomotor cost hypothesis (Pollux et al 2009), this morphological advantage of the placenta diminishes over the course of gestation. Superfetation may amplify this morphological advantage (Pollux et al 2009) (Fig.…”

Ecology and the diversification of reproductive strategies in viviparous fishes

“…Even though pregnancy in poeciliids has been experimentally linked to locomotor costs (Plaut 2002; Ghalambor et al . 2004), and there is evidence that matrotrophy increases streamlining (Fleuren et al . 2018) and is favored in high predation environments requiring efficient escape responses (Gorini-Pacheco et al .…”