Bioluminescence and repeated deep-sea colonization shaped the diversification and body size evolution of squaliform sharks.

Abstract

Understanding the underlying mechanisms that have generated the striking biodiversity inhabiting deep-sea ecosystems remains a challenge in evolutionary biology. Here, we addressed this topic by studying the macroevolutionary dynamics that have shaped the diversification of squaliform sharks, an iconic clade of deep-sea vertebrates. Using phylogenetic comparative methods and fossil-based Bayesian diversification estimates, both at species level, we combined fossil record data with molecular phylogenies to provide a quantitative framework for understanding the evolutionary history of Squaliformes. We reveal that early squaliform lineages originated in shallow water during the Early Cretaceous and experienced multiple independent shifts toward the deep sea during the Late Cretaceous. Importantly, we show that these shifts were likely facilitated by the acquisition of bioluminescence, which significantly impacted body size evolution among squaliform lineages. Furthermore, deep-sea colonization events coincide with periods of climate warming and marine transgression at the Cenomanian-Turonian and Palaeocene-Eocene transitions. Following these colonizations, deep-sea squaliform lineages have diversified over the last 30 Myr, resulting in one of the richest deep-sea radiations in sharks. These results demonstrate how the complex interplay between key innovation and colonization of new habitats drove major ecological transition, highlighting the importance of an integrative framework when studying deep-time macroevolutionary dynamics.