Evolutionary innovations such as eyes and live birth (viviparity) are dramatic, adaptive novelties that have shaped the evolutionary trajectories of animals. Viviparity is an important biological innovation that has required a set of complex phenotypic changes to allow internal incubation of embryos, radically changing the way in which organisms interact with their environment and transmit their genes to the next generation. As viviparity has evolved convergently hundreds of times in mammals, reptiles, fish, amphibians, and invertebrates, it is an ideal model to study evolutionary innovations, offering the opportunity to compare and contrast naturally replicated evolutionary experiments.
There are at least 23 independent origins of viviparity in fishes, with syngnathid fishes (seahorses and pipefish) unique in exhibiting male pregnancy. Male seahorses and pipefish have evolved specialized brooding pouches that provide protection, gas exchange, osmoregulation, and limited nutrient provisioning to developing embryos. Pouch structures differ widely across the Syngnathidae, offering an ideal opportunity to study the evolution of reproductive complexity. However, the physiological and genetic changes facilitating male pregnancy are largely unknown. We used transcriptome profiling to examine pouch gene expression at successive gestational stages in a syngnathid with the most complex brood pouch morphology, the seahorse Hippocampus abdominalis. Using a unique time-calibrated RNA-seq data set including brood pouch at key stages of embryonic development, we identified transcriptional changes associated with brood pouch remodelling, nutrient and waste transport, gas exchange, osmoregulation, and immunological protection of developing embryos at conception, development and parturition. Key seahorse transcripts share homology with genes of reproductive function in pregnant mammals, reptiles, and other live-bearing fish, suggesting a common toolkit of genes regulating pregnancy in divergent evolutionary lineages. Our work shows that there are common mechanisms that underpin the development of evolutionary innovations across divergent species.