Island biogeography and competition drive rapid venom complexity evolution across rattlesnakes

Understanding how human-mediated environmental change affects biodiversity and the timescale of an evolutionary response is key for conserving evolvability. Islands are proxies for fragmented landscapes and allow us to use historical changes in biodiversity under Island Biogeography Theory (IBT) to predict the consequences of immediate anthropogenic impacts on 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 congeneric competitors, island isolation, and island area best predicted variation in venom complexity. All variables exhibited a negative relationship with venom complexity, contrary to predictions for island area under IBT. Larger islands with more congeneric competitors exhibited reduced trait complexity, likely reflecting niche partitioning and venom specialization driven by interspecific competition and/or increases in habitat heterogeneity. Ultimately, we used a synthetic eco-evolutionary framework to predict functional trait evolution across fragmented and isolated habitats.