Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.

Summary Over the coming decades, our planet will experience a dramatic increase in average temperatures and an increase in the variance around those temperatures leading to more frequent and harsher heat waves. These changes will impact most species and impose strong selection on physiological traits. Rapid acclimation is the most direct way for organisms to respond to such extreme events, but we currently have little understanding of how the capacity to mount such plastic responses evolves. Accordingly, there is some urgency to determine how the physiological response to high temperatures varies within species, and how this variation is driven by the environment. Here, we investigate heat‐hardening capacity – a rapid physiological response that confers a survival advantage under extreme thermal stress – across 13 populations of a rain forest lizard, Lampropholis coggeri, from the tropics of north‐eastern Australia. Our results reveal that heat hardening is constrained in these lizards by a hard upper thermal limit for locomotor function (approximately 43 °C). Further, hardening response shows strong geographic variation associated with thermal environment: lizards from more predictable and more seasonal thermal environments exhibited greater hardening compared with those from more stochastic and less seasonal habitats. This finding – that predictability in thermal variation influences hardening capacity – aligns closely with theoretical expectations. Our results suggest that tropical species may harbour adaptive variation in physiological plasticity that they can draw from in response to climate change, and this variation is spatially structured in locally adapted populations. Our results also suggest that, by using climatic data, we can predict which populations contain particular adaptive variants; information critical to assisted gene flow strategies.

Ectothermic animals, such as amphibians and reptiles, are particularly sensitive to rapidly warming global temperatures. One response in these organisms may be to evolve aspects of their thermal physiology. If this response is adaptive and can occur on the appropriate time scale, it may facilitate population or species persistence in the changed environments. However, thermal physiological traits have classically been thought to evolve too slowly to keep pace with environmental change in longer‐lived vertebrates. Even as empirical work of the mid‐20th century offers mixed support for conservatism in thermal physiological traits, the generalization of low evolutionary potential in thermal traits is commonly invoked. Here, we revisit this hypothesis to better understand the mechanisms guiding the timing and patterns of physiological evolution. Characterizing the potential interactions among evolution, plasticity, behavior, and ontogenetic shifts in thermal physiology is critical for accurate prediction of how organisms will respond to our rapidly warming world. Recent work provides evidence that thermal physiological traits are not as evolutionarily rigid as once believed, with many examples of divergence in several aspects of thermal physiology at multiple phylogenetic scales. However, slow rates of evolution are often still observed, particularly at the warm end of the thermal performance curve. Furthermore, the context‐specificity of many responses makes broad generalizations about the potential evolvability of traits tenuous. We outline potential factors and considerations that require closer scrutiny to understand and predict reptile and amphibian evolutionary responses to climate change, particularly regarding the underlying genetic architecture facilitating or limiting thermal evolution.

The role of behavior in evolution has long been discussed, with some arguing that behavior promotes evolution by exposing organisms to selection (behavioral drive) and others proposing that it inhibits evolution by shielding organisms from environmental variation (behavioral inertia). However, this discussion has generally focused on the effects of behavior along a single axis without considering that behavior simultaneously influences selection in various niche dimensions. By examining evolutionary change along two distinct niche axes-structural and thermal-we propose that behavior simultaneously drives and impedes evolution in a group of Anolis lizards from the Caribbean island of Hispaniola. Specifically, a behavioral shift in microhabitat to boulders at high altitude enables thermoregulation, thus forestalling physiological evolution in spite of colder environments. This same behavioral shift drives skull and limb evolution to boulder use. Our results emphasize the multidimensional effects of behavior in evolution. These findings reveal how, rather than being diametrically opposed, niche conservatism and niche lability can occur simultaneously. Furthermore, patterns of niche evolution may vary at different geographic scales: because of thermoregulatory behavior, lizards at high and low elevation share similar microclimatic niches (consistent with niche conservatism) while inhabiting distinct macroclimatic environments (consistent with niche divergence). Together, our results suggest that behavior can connect patterns of niche divergence and conservatism at different geographic scales and among traits.

Understanding the motors and brakes that guide physiological evolution is a topic of keen interest, and is of increasing importance in light of global climate change. For more than half a century, Janzen’s hypothesis has been used to understand how climatic variability influences physiological divergence across elevation and latitude. At the same time, there has been increasing recognition that behavior and physiological evolution are mechanistically linked, with regulatory behaviors often serving to dampen environmental selection and stymie evolution (a phenomenon termed the Bogert effect). Here, we illustrate how some aspects of Janzen’s hypothesis and the Bogert effect can be connected to conceptually link climate, behavior, and rates of physiological evolution in a common framework. First, we demonstrate how thermal heterogeneity varies between nighttime and daytime environments across elevation in a tropical mountain. Using data from Hispaniolan Anolis lizards, we show how clinal variation in cold tolerance is consistent with thermally homogenous nighttime environments. Elevational patterns of heat tolerance and the preferred temperature, in contrast, are best explained by incorporating the buffering effects of thermoregulatory behavior in thermally heterogeneous daytime environments. In turn, climatic variation and behavior interact to determine rates of physiological evolution, with heat tolerance and the preferred temperature evolving much more slowly than cold tolerance. Conceptually bridging some aspects of Janzen’s hypothesis and the Bogert effect provides an integrative, cohesive framework illustrating how environment and behavior interact to shape patterns of physiological evolution.