Placental crises: disruptive selection and maternal under‐investment as the foundations of mammalian placental evolution and dysfunction

ABSTRACT Among the vertebrates, mammals are notable for the dominance of live birth and placental nutrition. The structural diversity of the mammalian placenta is remarkable, despite sharing a single common ancestor and conserved physiological functions. Historically, investigations into the evolution of the mammalian placenta have been grounded in ‘the efficiency paradigm’, i.e. the assumption that certain placental configurations permit easier nutrient exchange, but this paradigm has struggled to explain the diversity of mammalian placentation strategies. Here, we propose a new paradigm to understand mammalian placental evolution. Using multidimensional plotting of recorded placental structures, quantitative metrics for mammalian maternal investment, and illustrative computational modelling of physiological processes, we argue that the ancestral mammalian placenta is not a streamlined ‘highly efficient’ design, but rather a product of low maternal investment, with fitness costs that manifest as gestational demand increases. Expansion of small mammals into larger‐bodied, longer‐lived niches induces a ‘placental crisis’ characterised by maternal under‐investment and chronic gestational dysfunction, triggering an arms race through the interaction of disruptive selection and materno‐fetal conflict. We propose the acute severity of the placental crisis is the foundation of placental evolution. We go on to argue that some primates are currently in a state of placental crisis and that maternal under‐investment and inappropriate placentation are the evolutionary foundations of human gestational dysfunctions such as pre‐eclampsia. We conclude that the ancestral mammalian placenta was not an efficiently optimised design that allowed placentation to dominate the clade, but rather an idiosyncrasy of mammal‐specific biology, which likely hindered mammalian expansion into larger‐bodied niches.