Journal Article

The evolution of the placenta drives a shift in sexual selection in livebearing fish

Garland, T., Pollux, B. J. A., Springer, M. S., Meredith, R. W., Reznick, D. N.

2014

Overview

In poeciliid fish, the evolution of the placenta is associated with polyandry in females and correlates with a suite of phenotypic and behavioural traits in males. Consequences of placenta evolution Females laying eggs for external fertilization have no control over the quality of the offspring, and must rely on proxies of male quality such as courtship and display traits. Evolutionary theory holds that all this changed with the advent of the placenta: with low-cost eggs incubated internally, a mother can hedge her bets, inspecting the genetic quality of her mates directly and provisioning her embryos accordingly. The resulting mother–offspring conflict is expected to lead to polyandry (females mating with multiple males) and to males that are smaller, less showy and more prone to opportunistic or 'sneaky' mating. Here Bart Pollux et al . test these ideas by looking at the Poecilidae — guppies and their relatives — a family of fish in which the various species show all varieties of internal and external fertilization, and in which the placenta has evolved at least eight times independently. This approach allows the authors to confirm that the evolution of the placenta is associated with polyandry in females, and smaller, less showy males that have longer penises to facilitate more opportunities for opportunistic mating. The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent–offspring conflicts during pregnancy 1 , 2 , 3 , 4 . Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection 2 . This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation 5 , 6 . We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/181/2470 / Animal reproduction / Animals / Body Size / Cyprinodontiformes - anatomy & histology / Cyprinodontiformes - classification / Cyprinodontiformes - physiology / Eggs / Embryos / Evolution / Female / Females / Fish / Fishes / gene / Genitalia, Male - anatomy & histology / Humanities and Social Sciences / hypothesis / letter / Male / Males / maximum-likelihood / molecular phylogenetic-relationships / mosquitofish gambusia-holbrooki / multidisciplinary / Natural history / Offspring / parent-offspring conflict / Phylogenetics / Phylogeny / Physiological aspects / Placenta / poeciliidae cyprinodontiformes / Reproduction / reproductive mode / Science / Sexual behavior / Sexual Behavior, Animal - physiology / Sexual selection in animals / size dimorphism / Sperm / viviparity / Viviparity, Nonmammalian - physiology / Zoological research