Placental Evolution: Innovating how to Feed Babies.

ABSTRACT

The evolution of the placenta was transformative. It changed how offspring are fed during gestation from depositing all the resources into an egg to continually supplying resources throughout gestation. Placental evolution is infinitely complex, with many moving parts, but at the core it is driven by a conflict over resources between the mother and the baby, which sets up a Red Queen race, fueling rapid diversification of morphological, cellular, and genetic forms. Placentas from even closely related species are highly divergent in form and function, and many cellular processes are distinct. If we could extract the entirety of genomic information for placentas across all species, including the many hundreds that have evolved in fish and reptiles, we could find their shared commonality, and that would tell us which of the many pieces really matter. We do not have this information, but we do have clues. Convergent evolution mechanisms were repeatedly used in the placenta, including the intense selective pressure to co-opt an envelope protein to build a multinucleated syncytium, the use of the same hormones and structural proteins in placentas derived from separate embryonic origins that arose hundreds of millions of years apart, and the co-option of endogenous retroviruses to form capsids as a way of transport and as mutagens to form new enhancers. As a result, the placental genome is the Wild West of biology, set up to rapidly change, adapt, and innovate. This ability to adapt facilitated the evolution of big babies with big brains and will continue to support offspring and their mothers in our ever-changing global environment.