Testing the behavioral origins of novelty: did increased aggression lead to scale-eating in pupfishes?

Abstract

How novelty evolves is still largely unknown. Environmental changes are often assumed to precede novelty; however, behavioral shifts may also play a role. Here, we examine whether a shift in aggression explains the origin of a novel scale-eating pupfish species (Cyprinodon desquamator) within an adaptive radiation on San Salvador Island, Bahamas. We compared aggression using behavioral and gene expression data across three sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist), and additionally measured behavioral aggression in an outgroup generalist from North Carolina. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related genes in both the scale-eating and snail-eating species. Furthermore, male scale-eaters and female snail-eaters showed the highest levels of aggression compared to other groups. Differential gene expression in each specialist during larval development also suggested sex-mediated differences in male-male aggression and maternal care. Ultimately, our data indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization, mate competition, or selection on other ecologically relevant traits, including jaw size. Indeed, some adaptive variants associated with oral jaw size in the San Salvador radiation occur in genetic pathways with pleiotropic effects on aggression.