THE MESOZOIC-CENOZOIC SEXUAL REVOLUTION

The taxonomic and ecologic composition of the marine fauna shifted considerably during the late Mesozoic and Cenozoic. Here, we discuss an essential aspect of this marine revolution: sex. We divided marine animals into two groups: those that broadcast sperm into the water column and those that transfer sperm more or less directly between individuals via copulation or some other process (a small fraction of taxa could not be confidently assigned to either group). We analyzed the diversity history of these groups from the Ordovician to Neogene using shareholder quorum subsampling applied to marine animal genera in the Paleobiology Database. The diversity of broadcasters fluctuated without trend, reaching nearly identical peaks in the Devonian, Permian, and Cenozoic. Animals that transfer sperm fluctuated in diversity until the Cretaceous or Paleogene, when they radiated dramatically.

We argue that reproductive biology enhanced the radiation of these animals. When gametes are broadcast, fertilization success decreases rapidly with distance due to dilution, so reproduction is favored in large, dense populations. Direct transfer of sperm enhances fertilization success when individuals are rare, which could permit greater ecological specialization. Sperm transfer also introduces additional behavioral and anatomical mechanisms of reproductive isolation, which could enhance diversification. For these reasons, the increase in taxa that transfer sperm is probably mechanistically linked to increases in specialized ecological strategies like predation. The timing of the radiation may relate to factors like increased primary production, which could support more energetic, motile animals. The Cretaceous-Paleogene extinction probably played a role as well; animals that transfer sperm radiated dramatically in the Paleogene, and we suggest that they were able to speciate more rapidly in response to increased evolutionary opportunity in the aftermath of the extinction.

Interestingly, a similar argument has been made about the radiation of angiosperms on land; the transfer of pollen by animals rather than wind may have enhanced diversification and specialization. Together, these two radiations represent a global transformation in reproductive biology during the Cretaceous and Cenozoic.