Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

Abstract

The origins of novel trophic specialization, in which organisms begin to exploit novel resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate the behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics between groups. In this study, we investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while consuming shrimp and scales in the lab and found that scale-eating pupfish exhibited peak gape sizes that were twice as large as all other groups, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring the surface area removed per strike from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in 67% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale-biting. We also measured feeding kinematics of F1 hybrids to test whether feeding performance could contribute to reproductive isolation between species and found that F1 hybrid kinematics and performance more closely resembled those of generalists, suggesting that they may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale-eating.