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

Behavioral changes in a new environment are often assumed to precede the origins of evolutionary novelties. Here, we examined whether an increase in aggression is associated with a novel scale-eating trophic niche within a recent radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. We measured aggression using multiple behavioral assays and used transcriptomic analyses to identify differentially expressed genes in aggression and other behavioral pathways across 3 sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist) and 2 generalist outgroups. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related pathways in both the scale-eating and snail-eating specialists, despite their independent evolutionary origins. Increased behavioral aggression varied across both sex and stimulus context in both species. Our results indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization in general or mate competition. Alternatively, increased aggression may result from indirect selection on craniofacial traits, pigmentation, or metabolism—all traits which are highly divergent, exhibit signs of selective sweeps, and are affected by aggression-related genetic pathways which are differentially expressed in this system. In conclusion, the evolution of a novel predatory trophic niche within a recent adaptive radiation does not have clear-cut behavioral origins as previously assumed, highlighting the multivariate nature of adaptation and the complex integration of behavior with other phenotypic traits. Increased aggression does not sufficiently explain the behavioral origins of a novel scale-eating specialist in a recent adaptive radiation of Caribbean pupfishes. Both behavioral and transcriptomic data suggest that scale- and snail-eating pupfish have increased aggression compared to their generalist counterparts. Instead, increased aggression may have resulted from selection in other contexts, or from indirect selection on other traits (i.e., jaw size or pigmentation). In conclusion, the evolution of a novel predatory trophic niche does not have clear-cut behavioral origins as previously assumed.