Island biogeography and competition drive rapid venom complexity evolution across rattlesnakes

Abstract

Understanding how human-mediated environmental change affects biodiversity is key for conserving evolvability. Because the most severe impacts are ongoing, such an understanding is proving exceptionally difficult to attain. Islands are natural, replicated experiments that serve as proxies for habitat fragmentation and, therefore, allow us to use historical changes in biodiversity under Island Biogeography Theory (IBT) to predict the consequences of immediate anthropogenic impacts on functional trait evolution. Rattlesnake venoms are molecular phenotypes that mediate interactions with prey, and diet and venom complexity are positively correlated. Consequently, rattlesnake venoms allow us to investigate how functional traits co-vary with changes in biodiversity according to IBT. We collected venom from 83 rattlesnakes across multiple species and 11 islands in the Gulf of California and estimated venom complexity using the Shannon Diversity Index. Using a mixed effects modeling approach, we found that the number of congenerics, island isolation, and island area best predicted venom complexity variability. All variables exhibited a negative relationship with venom complexity, contrary to predictions for island area under IBT. Larger islands with more congenerics exhibited reduced trait complexity, perhaps reflecting niche partitioning and venom specialization. Ultimately, we used a synthetic eco-evolutionary framework to predict functional trait evolution across fragmented landscapes.