Evolutionary trade-offs between thermoregulatory behavior and thermal physiology in an assemblage of Sonoran desert lizards

Abstract

Predicting the responses of organisms to environmental change requires understanding the correlation between behavioral and physiological traits so as to avoid overheating without compromising performance. The concept of coadaptation, i.e., the correlation between thermoregulatory behavior and thermal physiology, is a foundational principle in evolutionary physiology. Yet, phylogenetic comparative analyses provide mixed support for coadaptation or evolutionary trade-offs. Few analyses of coadaptation between behavior and physiology include both a phylogenetic and an environmental context. Evidence for trade-offs maybe scarce, because the covariation between traits may be constrained by responses to local environmental conditions. Here we quantify how constraints in core thermal and behavioral trait may modulate patterns of coadaptation. We estimated thermoregulatory behavior and thermal physiology for 12 species of Phrynosomatid lizards inhabiting the Sonoran desert. We found low phylogenetic signal in traits associated with behavioral thermoregulation. Yes, behavioral traits have rates of evolution 3x higher than physiological traits associated with locomotor performance and temperature tolerance. When we modeled state-dependent shifts in thermal physiology as a function of thermoregulatory behavior, we found that thermoregulatory behavior did not influence the rate of evolution in thermal physiology. As environmental change may favor new combinations of behavioral and physiological traits, evolutionary mismatches between these traits can become exaggerated and result in novel phenotypic trajectories and result in a breakdown of thermal coadaptation. Our study revealed partial coadaptation and limited evidence for tradeoffs between thermoregulation and thermal physiology, which could be the default evolutionary pattern in the evolution of these traits, which has major implications for studying thermal coadaptation as environments change worldwide.