Heterochronic changes in gene expression underlie placental evolution in the fish family Poeciliidae

Abstract

Placentas evolved nine times in the fish family Poeciliidae. Each time, the egg follicle is the maternal contribution to the placenta. In non-placental species, the follicle fully provisions the egg before fertilization. In placental species, provisioning continues throughout development, and the follicle becomes a more elaborate, well-vascularized organ. We generated transcriptomes for follicles from yolking eggs and developing embryos from two pairs of closely related placental and non-placental species that represent independent origins of placentation plus one non-placental outgroup. We identified genes expressed in eggs but not embryos of non-placental species that continue to be expressed during embryonic development in placental species. Their functions include the maternal transfer of nutrients and immunity. We then reconstructed the ancestral state of the non-placental common ancestor of each species pair and identified genes that were either upregulated or downregulated in developing embryos of placental species relative to non-placental species. These include clusters associated with lipid metabolism, immune response and tissue structure. The two placental lineages were convergent in the function of these genes, but few genes were in common between them. Thus, diverse gene regulatory changes converge on shared essential functions in the independent origins of a complex trait.