Diversification of the eutherian placenta is associated with changes in the pace of life

Abstract

Few mammalian organs vary as dramatically among species as the placenta. This variation is remarkable considering that the placenta's primary function-transfer of nutrients and waste between mother and offspring-does not differ among species. Evolutionary changes in placental morphology remain poorly understood, with suggestions that parent-offspring conflict or evolutionary changes in life history might drive placental evolution. Here we demonstrate that life history differences among eutherian mammals are associated with major transitions in maternofetal interdigitation and placental invasiveness. We show that the repeated evolution of villous interdigitation is associated with reduced offspring production early in life and an increased lifespan. Further changes in placental morphology that reestablish a larger surface area are also associated with a change back to greater offspring production. After controlling for these differences in interdigitation, we also show that the least invasive placental type is associated with a fast pace of life. We predict that selection for a faster pace of life intensifies parent-offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the fetus and alter their relative allocation to offspring production across life.