Mechanisms of placental evolution: the genetics and physiology of pregnancy in lizards

Abstract

The placenta is a unique example of a complex organ that has evolved independently more than 115 times in amniotes (birds, reptiles, and mammals). Placentae exchange materials including respiratory gasses, nutrients, and hormones, between the mother and embryo. I aimed to identify the physiological and ecological factors that contribute to the evolution of placentation in vertebrates, focusing on the genetic mechanisms underpinning the evolution of placental functions, and the role of parent-offspring conflict in the evolution of placental traits. Given placentation has evolved independently many times, I assessed whether convergent evolution of placental functions is underpinned by the same genes in mammals and reptiles. I used high throughput sequencing to identify the gene expression patterns that facilitate placental functions in the placentotrophic southern grass skink (Pseudemoia entrecasteauxii).I show that hormone production occurs in the embryonic membranes of amniotes, and the production of growth factors by embryonic placental tissues is an exaptation of ancestrally expressed genes. I show that embryonic hormone production is a mechanism by which embryos can manipulate the function of the placenta, and regulate placental nutrient transport. By investigating the physiology and genetic underpinning of placental functions in reptiles, I provide fundamental data for understanding the evolution of viviparity and placentation in a lineage independent of viviparous mammals. I identify key similarities and differences between reptile and mammal pregnancy that outline the limits to which comparisons between the two lineages can be made. Finally, I show that parent offspring conflict is unlikely to play a role in the evolution of nutrient transport mechanisms in the placenta, but may be a driving force in the shift from lecithotrophic (a reliance on egg yolk for embryonic development) to placentotrophic nutrient provisioning through pregnancy.