Sex and the shifting biodiversity dynamics of marine animals in deep time

Significance

Fertilization mechanisms explain broad patterns in the taxonomic distribution of diversity in marine animals, as argued previously for land plants. We argue that fertilization via copulation (or some other significant interaction among adults) permits additional mechanisms of reproductive isolation and smaller population sizes relative to fertilization via the broadcasting of sperm into the water, thus enhancing diversification potential. Maximum-likelihood modeling of paleontological data indicates that the diversity of sperm broadcasters has been limited by diversity-dependent factors for the last 450 million years. In contrast, animals that copulate, etc., were also limited until the Cretaceous and then radiated dramatically, coincident with apparent major changes in marine productivity. Fertilization may have acted synergistically with ecological specialization in promoting diversification, particularly in predators.

Abstract

The fossil record of marine animals suggests that diversity-dependent processes exerted strong control on biodiversification: after the Ordovician Radiation, genus richness did not trend for hundreds of millions of years. However, diversity subsequently rose dramatically in the Cretaceous and Cenozoic (145 million years ago–present), indicating that limits on diversification can be overcome by ecological or evolutionary change. Here, we show that the Cretaceous–Cenozoic radiation was driven by increased diversification in animals that transfer sperm between adults during fertilization, whereas animals that broadcast sperm into the water column have not changed significantly in richness since the Late Ordovician (∼450 million years ago). We argue that the former group radiated in part because directed sperm transfer permits smaller population sizes and additional modes of prezygotic isolation, as has been argued previously for the coincident radiation of angiosperms. Directed sperm transfer tends to co-occur with many ecological traits, such as a predatory lifestyle. Ecological specialization likely operated synergistically with mode of fertilization in driving the diversification that began during the Mesozoic marine revolution. Plausibly, the ultimate driver of diversification was an increase in food availability, but its effects on the fauna were regulated by fundamental reproductive and ecological traits.