Estimates of molecular convergence reveal multiple genes with adaptive variation across teleost fish

Molecular convergence, where specific nonsynonymous changes in protein-coding genes lead to identical amino acid substitutions across multiple lineages, provides strong evidence of adaptive evolution. Detecting this signal across diverse taxa can reveal adaptive variation that may not be apparent when studying individual lineages. In this study, we search for convergent substitutions in the most speciose group of vertebrates, teleost fishes. Using an unsupervised approach, we detected convergence in 89 protein-coding gene families across 143 chromosomal-level genomes. To assess their functional implications, we integrate data on protein properties, gene expression across species and tissues, single-cell RNA sequencing of zebrafish embryonic development, and gene perturbation experiments in zebrafish. We found that, on average, the convergent genes had more gene copies as compared to background sets of genes. The convergent genes were associated with diverse processes including embryonic development, tissue morphogenesis, metabolism, and heat stress response. We found evidence that convergent substitutions were more radical than nonconvergent substitutions. When analyzing the expression of the convergent genes, we found that only one-third of them were tissue-specific, while the majority were expressed across multiple tissues and cell types. Genetic perturbation data further showed that the convergent genes can affect multiple structures across diverse tissues. These results highlight the important functional roles of the convergent genes, their potential pleiotropic nature, and suggest that they may underlie the evolution of lineage-specific adaptations in teleost fishes.