Heterochrony and Oophagy Underlie the Evolution of Giant Filter-Feeding Lamniform Sharks

Evolutionary transitions toward gigantic body sizes have profound consequences for the structure and dynamics of ecological networks. Among elasmobranchs (sharks and rays), gigantism has evolved on several occasions, most notably in the iconic Megalodon (Otodus megalodon†) and the extant whale shark (Rhincodon typus), basking shark (Cetorhinus maximus), and megamouth shark (Megachasma pelagios), all of which reach total lengths exceeding 6 m and, in some cases, reach 21 m or more. Comparative phylogenetic studies suggest that filter feeding and heterothermy provide two alternative evolutionary pathways leading to gigantism in sharks. These selection-based explanations for gigantism are important; however, our understanding of evolutionary transitions in body size is fundamentally constrained without a proximate, mechanistic understanding of how the suite of adaptations necessary to facilitate gigantism evolved. Here we propose the heterochrony hypothesis for the evolution of the giant filter-feeding shark ecomorphotype. We suggest that craniofacial adaptations for oophagy in embryonic stages of lamniform sharks are retained through ontogeny in C. maximus and M. pelagios by paedomorphosis, resulting in an enlarged head and mouth relative to the rest of the body, even in adulthood. This change in developmental timing enables these taxa to optimize prey acquisition, which is thought to be the limiting factor for the evolution of gigantism in filter-feeding marine vertebrates. We discuss the concordance of this hypothesis with current developmental, morphological, and evolutionary data, and we suggest future means by which the hypothesis could be tested.