The genomic basis of independent marine transitions in turtles: convergent episodic adaptation and demographic shifts

Abstract

The transition from terrestrial to marine environments represents one of the most fundamental evolutionary shifts in vertebrate history, requiring radical physiological and genomic remodeling. We investigated the genomic signatures of saltwater adaptation in the green sea turtle (Chelonia mydas), the leatherback turtle (Dermochelys coriacea), and the independently evolved estuarine diamondback terrapin (Malaclemys terrapin). Our analyses reveal that the marine transition is characterized by rapid evolution and expansion in gene families linked to iron metabolism, organ morphogenesis, and sensory perception—patterns that mirror those seen in other secondarily marine tetrapods. Notably, while we identified shared targets of positive selection across these independent lineages, we found no evidence of repeated evolution at the nucleotide level, reinforcing that functional convergence often arises through distinct molecular trajectories. Furthermore, demographic reconstructions reveal that saltwater-adapted turtles share a history of deep-time population declines; however, the delayed recovery of M. terrapin underscores the specific susceptibility of estuarine specialists to Pleistocene sea-level volatility. By bridging comparative genomics and historical demography, this study provides new insights into the genomic basis of marine adaptations in turtles and a comprehensive framework for understanding the molecular and ecological mechanisms that facilitate major vertebrate transitions into the marine realm.