A post-embryonic specific and ecologically selective network underlies metamorphic remodelling in teleosts

Evolutionary developmental biology has primarily focused on embryogenesis. Yet, much of the diversity in animal form and function emerges during post-embryonic developmental transitions such as metamorphosis. Whether these transitions share a conserved genetic architecture, and how that architecture evolves remains unclear. In this study we use a comparative framework and multiple data modalities to characterise post-embryonic development in five species of teleost fish. Despite 200 million years of divergence, we uncover a post-embryonic developmental gene network conserved in all five species. This network comprises core cellular process modules shared with embryogenesis, and developmental remodelling modules unique to post-embryonic development. Both sets have highly conserved expression and tissue specificity patterns across several teleost species and the outgroup spotted gar. The network is broadly responsive to thyroid hormone treatments, yet its response to ecological variation is focussed and selective. Although largely conserved at the coding sequence level, the network has undergone significant turnover in gene family copy number following the teleost-specific whole-genome duplication. Across teleosts, the copy number variation is associated with macroevolutionary variation in a number of ecological and morphological traits such as trophic level and swimming performance. Multi-species tissue expression, and zebrafish perturbation phenotypes provide support for these associations. Our results reveal an ancient, endocrine controlled network underlying post-embryonic development in teleosts. It suggests a conserved, yet evolvable genetic architecture can be redeployed, refined, and repurposed to generate diversity in form and function.