Comparative genomic analyses of trans-ithmanian reef fishes reveals different molecular targets of environmental adaptation in different families.

The extent to which selection acts upon the same molecular targets when faced with the same environmental changes has important implications for our understanding of the repeatability and predictability of evolutionary processes. Replicated natural experiments are well positioned to provide insight, however often these involve closely related species or populations of the same species. Given that the similarity of genetic background makes the same molecular change more likely, it is essential to evaluate the extent to which molecular parallelism occurs in more distantly related species. The rise of the Isthmus of Panama presents an ideal natural experiment to investigate the prevalence of parallel molecular changes in distantly related lineages exposed to the same environmental regimes of temperature, salinity and primary productivity in the two newly formed oceans. Here, we generate high-quality reference genomes for two replicate pairs of geminate reef fishes, one in the family Pomacentridae and one in the Serranidae. Comparative analyses of positive selection in protein-coding genes and of gene family evolution revealed multiple signals of potentially adaptive divergence between geminate species in response to environmental regime. Common targets of selection between families included MAPK signalling ( MAP3K10 ), solute transport ( SLC46A2 ) and reproduction ( ZPL3L ), as well as expansions in immune and MAPK related gene families. Overall, however, we found minimal evidence of parallelism between families either at the gene level or when considering higher functional categories. Our findings suggest that phylogenetic constraints may limit the levels of molecular parallelism in distant lineages even when faced with comparable selective pressures.