Evolutionary pathways toward gigantism in sharks and rays.

Abstract

Through elasmobranch (sharks, skates and rays) evolutionary history, gigantism evolved multiple times in phylogenetically distant species, some of which are now extinct. Interestingly, the world’s largest sharks display two specializations found never to overlap: filter-feeding and mesothermy. The contrasting lifestyles of elasmobranch giants provide an ideal case study to elucidate the evolutionary pathways leading to gigantism in the oceans. Here, we applied a phylogenetic approach to a global dataset of 459 taxa to study the evolution of elasmobranch gigantism. We found that filter feeders and mesotherms deviate from general relationships between trophic level and body size and exhibit significantly larger sizes than other elasmobranchs. We confirm that filter-feeding arose multiple times during the Paleogene, and suggest the possibility of a single origin of mesothermy in the Cretaceous. Together, our results elucidate three evolutionary pathways that enable gigantism: mesothermy, filter-feeding and ectothermic-macropredation. The mesothermic and filter-feeding pathways were followed by ancestrally large clades and facilitated extreme sizes through specializations for enhancing prey intake. Species following the ectothermic-macropredatory pathway did not acquire these specializations, and are correspondingly constrained to the lower limits of gigantism. Importantly, the very adaptive strategies that enabled the evolution of the largest sharks are highly vulnerable to extinction.