Adaptive Evolution of Animal Proteins over Development: Support for the Darwin Selection Opportunity Hypothesis of Evo-Devo

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A driving hypothesis of evolutionary developmental biology is that animal morphological diversity is shaped both by adaptation and by developmental constraints. Here, we have tested Darwin’s “selection opportunity” hypothesis, according to which high evolutionary divergence in late development is due to strong positive selection. We contrasted it to a “developmental constraint” hypothesis, according to which late development is under relaxed negative selection. Indeed, the highest divergence between species, both at the morphological and molecular levels, is observed late in embryogenesis and postembryonically. To distinguish between adaptation and relaxation hypotheses, we investigated the evidence of positive selection on protein-coding genes in relation to their expression over development, in fly Drosophila melanogaster, zebrafish Danio rerio, and mouse Mus musculus. First, we found that genes specifically expressed in late development have stronger signals of positive selection. Second, over the full transcriptome, genes with evidence for positive selection trend to be expressed in late development. Finally, genes involved in pathways with cumulative evidence of positive selection have higher expression in late development. Overall, there is a consistent signal that positive selection mainly affects genes and pathways expressed in late embryonic development and in adult. Our results imply that the evolution of embryogenesis is mostly conservative, with most adaptive evolution affecting some stages of postembryonic gene expression, and thus postembryonic phenotypes. This is consistent with the diversity of environmental challenges to which juveniles and adults are exposed.