I'm a post-doc at the Smithsonian Tropical Research Institute in Panama. I'm primarily interested in questions related to thermal adaptation in terrestrial ecotherms.
Parasites are an ever-present threat to the organisms they interact with. Reptiles, like anoles, are often heavily infested with mites, an ectoparasite that drinks the lizard’s blood and are often visible on the surface of the skin. Despite the ubiquity of mite infestations on reptiles, the fitness costs of these infestations and the factors that cause mite load to vary among individuals within populations are surprisingly understudied.
Adam Rosso, a masters student in Christian Cox’s lab at Georgia Southern University, studied the factors that drive variation in mite infestation among individuals in a population of slender anoles (Anolis apletophallus) in Panama. Slender anoles are sexually dimorphic; males have much larger dewlaps than females. Adam counted mite loads on hundreds of lizards and asked a series of questions, including: How does mite load differ between the sexes? Do the sexes differ in where they are being parasitized on their bodies? Can ecological factors such as habitat use and body temperature affect mite load?
First, Adam found that males have more mites than females, but this was due entirely to their larger dewlaps. In fact, females actually had more mites on other parts of their bodies (such as on their hind and forelimbs). But it gets even more interesting: Adam found that mite infestation increases with dewlap area in males but not in females, suggesting that mites prefer male dewlaps over female dewlaps. Neither field-active body temperature nor perch characteristics predicted mite loads in either sex, suggesting that dewlaps are the main factor influencing ectoparasitism in this population. Adam’s results suggest that there may be an important cost to producing a large dewlap in males. More generally, if parasite loads and dewlap sizes are seen as honest signals in anoles, the results of Adam’s work could have implications for understanding sexual selection and morphological evolution in this group of lizards.
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.
The Bay Islands proper consist of a crescent of four land-bridge islands lying approximately 50 km off the northern coast of Honduras in the Caribbean Sea. About halfway between those islands and the coast lies a smaller sub-archipelago, known as the Cayos Cochinos (or ‘Hog Islands’), which consist of two larger islands (Cayo Mayor and Cayo Menor) and 13 smaller cays (see the map below). The Cayos Cochinos are famous in the commercial reptile trade for their endemic populations of insular-dwarf ‘pink’ boa constrictors.
The Bay Islands and Cayos Cochinos of Honduras. For scale, Cayo Menor and Cayo Mayor are about 3 km apart. Adapted from Green (2010).
I’ve had the pleasure of conducting herpetological research in the Bay Islands since 2007 thanks to support from a UK-based conservation organization called Operation Wallacea, and a generous team of researchers (Chad Montgomery, Bob Reed, Scott Boback, Steve Green, and Tony Frazier) that have been working on the boa and Ctenosaura populations there for several years, and were nice enough to get me involved. And while the Bay Islands have gained some notoriety for their exotic snakes, another local squamate has gone (almost) entirely unnoticed. I’m alluding to, of course, the anoles. In 2007, when I was helping Chad Montgomery with his Ctenosaura melanosterna project on Cayo Menor, I began to notice just how abundant the anoles on that island were. The little guys seemed to be on almost every tree in the interior of the island. After asking around and doing a few literature searches, I started to realize just how untouched, and potentially interesting, this system really was.
Two anole species occur in the Cayos Cochinos, Anolis lemurinus and Anolis allisoni.
