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

Abstract

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. Significance StatementUnderstanding the extent to which species exposed to similar environmental conditions may adapt using similar genetic solutions has important implications for our understanding of evolutionary processes and how we may expect species to adapt in the future. However, systems where multiple, independent lineages are faced with the same shift in conditions are rare. The rise of the Isthmus of Panama provides a unique, natural experiment where multiple marine species have been divided and exposed to radically different environmental conditions. Here, we generate genomes for separated species in two distantly related families of reef fishes and compare genome-wide patterns of divergence. Our analyses identified signals of selection in protein-coding genes and shifts in gene family size consistent with adaptation to the distinct environments, however the specific genes and pathways involved predominantly differed between the families, revealing that, even under shared selective pressures, molecular mechanisms may differ across more distant lineages.