Climate cooling and clade competition likely drove the decline of lamniform sharks

Abstract

Understanding heterogeneity in species richness between closely related clades is a key research question in ecology and evolutionary biology. Multiple hypotheses have been proposed to interpret such diversity contrasts across the tree of life, with most studies focusing on speciation rates to explain clades' evolutionary radiations, while often neglecting extinction rates. Here we study a notorious biological model as exemplified by the sister relationships between mackerel sharks (Lamniformes, 15 extant species) and ground sharks (Carcharhiniformes, ∼290 extant species). Using a comprehensive fossil dataset, we found that the diversity dynamics of lamniforms waxed and waned following repeated cycles of radiation phases and declining phases. Radiation phases peaked up to 3 times the current diversity in the early Late Cretaceous. In the last 20 million years, the group declined to its present-day diversity. Along with a higher extinction risk for young species, we further show that this declining pattern is likely attributed to a combination of abiotic and biotic factors, with a cooling-driven extinction (negative correlation between temperature and extinction) and clade competition with some ground sharks. Competition from multiple clades successively drove the demise and replacement of mackerel sharks due to a failure to originate facing the rise of ground sharks, particularly since the Eocene. These effects came from ecologically similar carcharhiniform species inhibiting diversification of medium- and large-sized lamniforms. These results imply that the interplay between abiotic and biotic drivers had a substantial role in extinction and speciation, respectively, which determines the sequential rise and decline of marine apex predators.