An evolvable and functionally partitioned network underlies developmental remodelling in teleosts

Comparative embryology has revealed that early animal development is based on highly conserved genetic programs. Beyond embryogenesis however, animals undergo remarkably diverse post-embryonic developmental transitions such as metamorphosis. Whether these transitions are also organised into conserved genetic programs remains largely unexplored. To identify conserved genetic programs underlying post-embryonic development, we examine metamorphic remodelling in five teleost fishes, spanning 200 million years of evolution. By integrating comparative co-expression networks, evolutionary genomics, phylogenetic modelling, and functional data in zebrafish, we uncovered a conserved post-embryonic developmental network. This conserved network comprises components involved in core cellular processes, and involved in development and physiology, both of which are under the control of thyroid hormone during metamorphosis. Despite evolutionary conservation at the coding sequence level, this network exhibits significant turnover in gene family copy number following the teleost-specific whole-genome duplication as well as lineage-specific expansions and contractions. The variation in gene copy numbers is associated with macroevolutionary variation in a number of ecological and morphological traits, including swimming performance, and trophic level. Cross-species tissue expression, zebrafish single-cell transcriptomics, and zebrafish perturbation phenotypes placed the implicated genes in biological contexts relevant to these traits. Together, our results provide evidence of an ancient, functionally partitioned post-embryonic developmental network that has diversified throughout teleost evolution. The heterochronic variation in network function, changes in endocrine activity, and gene-family turnover provide potential routes through which a shared developmental architecture contributed to the evolution of phenotypic diversity in teleosts.