Why do placentas evolve? A test of the life‐history facilitation hypothesis in two clades in the genus Poeciliopsis representing two independent origins of placentas

Abstract

Summary Most of what we know about placentas comes from mammals, yet little can be learned from them about the adaptive significance of the placental mode of reproduction because they all derived their placenta from a single common ancestor that lived over 100 million years ago. We can make inferences about the adaptive significance of placentation from fish in the family Poeciliidae because there have been multiple, recent origins of placentation, affording an opportunity to compare close relatives with and without placentas and to seek properties that are common to each origin of placentation. Here, we used field collections and a common garden study to quantify the degree of placentation and related it to aspects of the life history in two clades of live‐bearing fish from the genus Poeciliopsis that each contains an independent origin of placentation. Doing so enables us to test the ‘life history facilitation hypothesis’, or the proposal that the placenta evolved to facilitate the evolution of some other feature of the life history. We found that the evolution of placentation in each clade is tightly correlated with the evolution of other components of the life history, but that the nature of the association is radically different across the two clades. In the Northern Clade the magnitude of post‐fertilization maternal provisioning is negatively correlated with age at maturity, mass at maturity, offspring dry mass and interlitter interval. In contrast, degree of matrotrophy in the Southern Clade is positively correlated with age at maturity, mass at maturity, offspring dry mass and inter‐litter interval. There is thus no consistent relationship between the evolution of placentas and other features of the life history, which negates those proposals that the placenta evolved to facilitate the evolution of other features of the life history. However, there is a negative correlation between degree of placentation and ovary dry mass and reproductive allocation common to both clades, suggesting that placentation may be an adaptation that facilitates a reduction in reproductive allocation.