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

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.

Plate tectonic regulation of global marine animal diversity

“…The specific Phanerozoic trajectory of marine animal genus richness remains contested (11,13,(15)(16)(17)21), but analyses consistently reproduce several long-term patterns. A quick rise to a volatile Paleozoic plateau (19), a drop during the end-Permian, a prolonged Early Mesozoic recovery, and a subsequent rise (9,(20)(21)(22) that eventually exceeded the Paleozoic maximum in the Late Mesozoic or Early Cenozoic ( Fig. 2 A and B) are all consistent features of the paleontological literature.…”

“…Changing productivity patterns (8), coevolutionary dynamics (9), latitudinal biodiversity gradients (48), incumbency and invasibility dynamics (56), and morphological/ecological character displacement (57) may all be facilitated or triggered by changing geographic connectivity. Even biotic hypotheses that do not have an obvious connection to the geographic arrangement of continental crust, such as the emergence of sexual characteristics (22), are, at worst, independent of the tectonic dynamics presented here and should not be considered mutually exclusive. Nevertheless, our results do provide compelling evidence that the shifting distribution and connectivity of continental landmass, either as the primary forcer or as a complement to other macroevolutionary processes, has been a fundamental driver of long-term global Phanerozoic biodiversity patterns.…”

“…Although biodiversity also appears to be in a declining phase (Fig. 2), it is not clear to what extent this decline reflects an actual downturn in biodiversity (22,49) versus idiosyncratic paleontological sampling of the tropics (39).…”

“…Without the end-Permian mass extinction, the Paleozoic biodiversity plateau (51) would likely have persisted until the start of the next fragmentation regime. Second, if coalescence does serve to stabilize biodiversity, then the increase in genus richness observed during the Cenozoic will likely slow or cease sometime in the relatively near future (22,49). A new interval of plate aggregation has been underway since the Late Cretaceous; this also suggests that any downturn in present-day taxonomic richness (52) may be followed by a protracted recovery phase that is more analogous to the Triassic than it is to the Paleogene, at least from the perspective of long-term plate tectonic boundary conditions.…”

“…Nevertheless, many major features in the fossil record of biodiversity are consistently reproducible, although not all have universally accepted explanations. In particular, the reasons for a long Paleozoic plateau in marine richness and a steady rise in biodiversity during the Late Mesozoic-Cenozoic remain contentious (11,12,14,(19)(20)(21)(22).…”