High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays

Abstract

One of the great mysteries of evolutionary biology is why closely related lineages accumulate species at different rates. Theory predicts that populations undergoing strong sexual selection will more quickly differentiate because of increased potential for genetic isolation [1-6]. Whether or not these population genetic processes translate to more species at macroevolutionary scales remains contentious [7]. Here we show that lineages with bioluminescent courtship, almost certainly a sexually selected trait, have more species and faster rates of species accumulation than their non-luminous relatives. In each of ten distantly related animal lineages from insects, crustaceans, annelid worms, and fishes, we find more species in lineages with bioluminescent courtship compared to their sister groups. Furthermore, we find under a Yule model that lineages with bioluminescent courtship displays have significantly higher rates of species accumulation compared to a larger clade that includes them plus non-luminous relatives. In contrast, we do not find more species or higher rates in lineages that use bioluminescence for defense, a function presumably not under sexual selection. These results document an association between the origin of bioluminescent courtship and increased accumulation of species, supporting theory predicting sexual selection increases rates of speciation at macroevolutionary scales to influence global patterns of biodiversity.

Speciation is associated with changing ornamentation rather than stronger sexual selection

“…; Seddon et al. ; Huang and Rabosky ; but see Ellis and Oakley for the case of bioluminescent animals). A neglected possibility is that any change in sexual ornamentation, including decreases or losses of ornamentation, might also promote reproductive isolation and that, as a consequence, it is not the strength of sexual selection that predicts speciation, but the extent of evolutionary changes in ornamentation (Cardoso and Mota ).…”

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

“…Whether fertilization is internal or external, adults must recognize each other and interact directly, and reproductive isolation is driven not just by gametic incompatibility, habitat separation, and the like but also by behavioral and anatomical barriers at the adult level (e.g., courtship rituals, physical inability to copulate) (28)(29)(30)(31)(32). Behavioral barriers to gene flow and sexual selection are generally believed to facilitate speciation (15,(33)(34)(35), and reduced Allee effects may permit species to survive, even if rare. To the extent that animals are adept at recognizing and mating with members of their own species, they would be analogous to orchids, where pollen delivery is more species-specific than with many other plants (20,21).…”

Love, not war, drove the Mesozoic marine revolution

“…Genetic surveys of marine invertebrates demonstrate that copulating species have greater genetic diversity and less inbreeding than broadcast spawners (21). Sexually selected and courting animal species are well established to have higher speciation rates relative to other lineages (27). But active selection of sexual partners has been demonstrated to not be sufficient, by itself, to result in increased speciation rates (20,28); additional factors are required to prime the diversity pump, including ecological specialization and environmental opportunity.…”