Parallel genomic changes drive repeated evolution of placentas in live-bearing fish

The evolutionary origin of complex organs defies empirical study because most evolved hundreds of millions of years ago. The placenta of live-bearing fish in the family Poeciliidae represents a unique opportunity to study the origin of complexity : in this family, placentas evolved at least nine times, vary in the scope of their development and are sometimes of recent origin, with closely related species with and without placentas. It is currently unknown whether convergent genomic changes underlie this repeated evolution. Here we compare whole genomes of 26 poeciliid species representing six independent origins of placentation. We show that the evolution of placentas is accompanied by convergent changes in the evolutionary rate of both protein-coding genes, as well as convergent changes in non-coding regulatory elements. Shifts in evolutionary rate that correlate with placentation were mainly observed in transporter- and vesicle-located genes, while shuffling of regulatory elements occurred mainly around developmental genes. We conclude that convergent genomic changes in both protein-coding and regulatory regions may underlie the repeated evolution of the placenta in the Poeciliidae.