Comparative genomics supports ecologically induced selection as a putative driver of banded penguin diversification

Abstract

The relative importance of genetic drift and local adaptation in facilitating speciation remains unclear. This is particularly true for seabirds, which can disperse over large geographic distances, providing opportunities for intermittent gene flow among distant colonies that span the temperature and salinity gradients of the oceans. Here, we delve into the genomic basis of adaptation and speciation of banded penguins, Galápagos (Spheniscus mendiculus), Humboldt (Spheniscus humboldti), Magellanic (Spheniscus magellanicus), and African penguins (Spheniscus demersus), by analyzing 114 genomes from the main 16 breeding colonies. We aim to identify the molecular mechanism and genomic adaptive traits that have facilitated their diversifications. Through positive selection and gene family expansion analyses, we identified candidate genes that may be related to reproductive isolation processes mediated by ecological thermal niche divergence. We recover signals of positive selection on key loci associated with spermatogenesis, especially during the recent peripatric divergence of the Galápagos penguin from the Humboldt penguin. High temperatures in tropical habitats may have favored selection on loci associated with spermatogenesis to maintain sperm viability, leading to reproductive isolation among young species. Our results suggest that genome-wide selection on loci associated with molecular pathways that underpin thermoregulation, osmoregulation, hypoxia, and social behavior appears to have been crucial in local adaptation of banded penguins. Overall, these results contribute to our understanding of how the complexity of biotic, but especially abiotic, factors, along with the high dispersal capabilities of these marine species, may promote both neutral and adaptive lineage divergence even in the presence of gene flow.