A male brown anole from the island of Great Exuma in The Bahamas.
Human-caused climate change is rapidly changing the thermal environments experienced by many species. Most ectotherms, like many of our beloved anoles, maintain small home ranges and are therefore assumed to lack the ability to disperse over long distances. If they can’t migrate to thermally suitable areas, how will anole populations deal with climate change? A major theme emerging in the literature is that evolutionary adaptation may be one of the primary ways that anoles compensate for rapid environmental change.
In close collaboration with many other people, my recent work has focused on thermal adaptation in the brown anole (Anolis sagrei) from The Bahamas. Our early findings suggested that this species may be able to rapidly adapt to changing thermal environments. For example, we found that the thermal optimum for running speed (the “thermal performance curve”) was locally adapted in populations living on a series of thermally variable cays in The Bahamas. Populations were locally adapted despite high levels of gene flow across the archipelago, suggesting that selection is constantly weeding out maladapted genotypes as they arrive and favoring individuals whose thermal biology matched local conditions. We also tested this idea experimentally by transplanting brown anoles from a cool, forested environment to a sun-baked peninsula and tracking (through mark-recapture) which individuals survived and which perished. The peninsula was much warmer and more thermally variable than the ancestral environment, and we were able to show that strong selection favored individuals with higher thermal optima and broader thermal tolerances on the peninsula. While these studies suggested that there is potential for evolutionary adaptation to future climate change, a major question was left unanswered: is there sufficient genetic variation underlying thermal traits such that populations could evolve rapidly? If a trait is not heritable, it will not evolve, and surprisingly few studies have measured the additive genetic basis of physiological traits in lizards.
To answer this question, we captured adult brown anoles from the same two populations involved in our previous transplant experiment (lizards from the islands of Eleuthera and Great Exuma in The Bahamas), brought them back to Bob Cox’s lab at the University of Virginia, and conducted a common-garden breeding experiment. First, Bob raised hundreds of offspring from these two populations, which were native to environments that differed dramatically in their thermal properties. The environment on Eleuthera was much warmer and more thermally variable than the environment on Exuma, so if genetic adaptation had occurred, the offspring of these populations should differ in their thermal physiology when raised in an identical environment, and the differences should be congruent with our previous estimates of natural selection. Interestingly, we found that these populations differed in every aspect of thermal physiology that we measured, but only some of these differences matched our predictions. For example, Eleuthera offspring had higher thermal optima for running speed (predicted to occur based on the warm environment they came from), but lower performance breadths (the opposite of what we predicted because the site on Eleuthera is more thermally variable).
Next, to understand the potential for rapid adaptation to future climate change, we used the pedigrees of the breeding colonies to estimate the additive genetic basis (i.e. heritability) of both the thermal sensitivity of running speed and several aspects of thermoregulatory behavior. For the latter, Don Miles introduced hundreds of Great Exuma individuals to a thermal gradient and measured how they behaved in the gradient. Though the results were somewhat variable, the bottom line is that we found very low heritability in most aspects of thermal physiology and thermoregulatory behavior.
The thermal sensitivity of running speed differed between brown anole populations from the cooler island of Exuma and the hotter island of Eleuthera, even when we raised hatchlings in an identical environment, suggesting that the populations have genetically diverged. Peak running speed for Eleuthera lizards occured at warmer body temperatures, and Exuma individuals ran faster at all body temperatures measured other than the lowest. This figure is copied from Logan et al. (2018).
In general, our results suggest that these populations have adapted to divergent thermal environments in the past, but lack the capacity to evolve rapidly into the future. This could be because strong selection has reduced genetic variation in thermal traits by fixing locally adapted alleles in each environment. Or in the case of the thermal performance curves, it is possible that precise thermoregulatory behavior has removed the need for alleles that confer broad thermal tolerance, leading to mutational decay of those genes. Whatever the cause, we now have evidence to suggest that some thermal traits in brown anoles lack the capacity to evolve rapidly.
There are a number of caveats that go along with our study. First, our sample sizes (Great Exuma = 289, Eleuthera = 119) are modest as quantitative genetic studies go. That fact combined with the difficulty of getting precise estimates of physiological and behavioral traits means that our study should not be considered the final word on the evolutionary potential of thermal performance curves or thermoregulatory behavior in brown anoles or any other species. Second, brown anoles are one of the most successful species on the planet. Indeed, they are extremely common in their native range and have invaded much of the Western Hemisphere. This is not a species that appears to have trouble conquering novel thermal environments, so in no way are we suggesting that they are particularly vulnerable to climate change. In fact, our data suggests that they are likely using behavioral adjustments or phenotypic plasticity to adapt to novel environments, and if anything testifies to the fact that within-generation physiological adjustments can be an extremely powerful tool for mitigating the effects of climate change. Lastly, there are a number of traits we did not measure. What about the critical thermal limits? What about the thermal sensitivity of other performance traits like digestive efficiency, endurance, and bite force? What about thermoconforming species that live deep in forests and have different thermoregulatory strategies and physiological tendencies? There is a lot of work left to be done before we know the full evolutionary potential of anoles under rapid climate change.
The work I’ve discussed here resulted from the efforts of a number of hard-working scientists, including Ryan Calsbeek, Bob Cox, Joel McGlothlin, Don Miles, Katie Duryea, John David Curlis, Anthony Gilbert, Albert Chung, Orsolya Molnar, and Benji Kessler.
