Sustained Drought, but Not Short-Term Warming, Alters the Gut Microbiomes of Wild Anolis Lizards.

As rising temperatures threaten biodiversity across the globe, tropical ectotherms are thought to be particularly vulnerable due to their narrow thermal tolerance ranges. Nevertheless, physiology-based models highlighting the vulnerability of tropical organisms rarely consider the contributions of their gut microbiota, even though microbiomes influence numerous host traits, including thermal tolerance. We combined field and lab experiments to understand the response of the slender anole lizard (Anolis apletophallus) gut microbiome to climatic shifts of various magnitude and duration. First, to examine the effects of long-term climate warming in the wild, we transplanted lizards from the mainland Panama to a series of warmer islands in the Panama Canal and compared their gut microbiome compositions after three generations of divergence. Next, we mimicked the effects of a short-term "heat-wave" by using a greenhouse experiment and explored the link between gut microbiome composition and lizard thermal physiology. Finally, we examined variation in gut microbiomes in our mainland population in the years both before and after a naturally occurring drought. Our results suggest that slender anole microbiomes are surprisingly resilient to short-term warming. However, both the taxonomic and predicted functional compositions of the gut microbiome varied by sampling year across all sites, suggesting that the drought may have had a regional effect. We provide evidence that short-term heat waves may not substantially affect the gut microbiota, while more sustained climate anomalies may have effects at broad geographic scales. IMPORTANCE As climate change progresses, it is crucial to understand how animals will respond to shifts in their local environments. One component of this response involves changes in the microbial communities living in and on host organisms. These "microbiomes" can affect many processes that contribute to host health and survival, yet few studies have measured changes in the microbiomes of wild organisms experiencing novel climatic conditions. We examined the effects of shifting climates on the gut microbiome of the slender anole lizard (Anolis apletophallus) by using a combination of field and laboratory studies, including transplants to warm islands in the Panama Canal. We found that slender anole microbiomes remain stable in response to short-term warming but may be sensitive to sustained climate anomalies, such as droughts. We discuss the significance of these findings for a species that is considered highly vulnerable to climate change.

Sex-specific microhabitat use is associated with sex-biased thermal physiology in Anolis lizards.

If fitness optima for a given trait differ between males and females in a population, sexual dimorphism may evolve. Sex-biased trait variation may affect patterns of habitat use, and if the microhabitats used by each sex have dissimilar microclimates, this can drive sex-specific selection on thermal physiology. Nevertheless, tests of differences between the sexes in thermal physiology are uncommon, and studies linking these differences to microhabitat use or behavior are even rarer. We examined microhabitat use and thermal physiology in two ectothermic congeners that are ecologically similar but differ in their degree of sexual size dimorphism. Brown anoles (Anolis sagrei) exhibit male-biased sexual size dimorphism and live in thermally heterogeneous habitats, whereas slender anoles (Anolis apletophallus) are sexually monomorphic in body size and live in thermally homogeneous habitats. We hypothesized that differences in habitat use between the sexes would drive sexual divergence in thermal physiology in brown anoles, but not slender anoles, because male and female brown anoles may be exposed to divergent microclimates. We found that male and female brown anoles, but not slender anoles, used perches with different thermal characteristics and were sexually dimorphic in thermal tolerance traits. However, field-active body temperatures and behavior in a laboratory thermal arena did not differ between females and males in either species. Our results suggest that sexual dimorphism in thermal physiology can arise from phenotypic plasticity or sex-specific selection on traits that are linked to thermal tolerance, rather than from direct effects of thermal environments experienced by males and females.

Ectoparasite extinction in simplified lizard assemblages during experimental island invasion.

Introduced species can become invasive, damaging ecosystems and disrupting economies through explosive population growth. One mechanism underlying population expansion in invasive populations is 'enemy release', whereby the invader experiences relaxation of agonistic interactions with other species, including parasites. However, direct observational evidence of release from parasitism during invasion is rare. We mimicked the early stages of invasion by experimentally translocating populations of mite-parasitized slender anole lizards (Anolis apletophallus) to islands that varied in the number of native anoles. Two islands were anole-free prior to the introduction, whereas a third island had a resident population of Gaige's anole (Anolis gaigei). We then characterized changes in trombiculid mite parasitism over multiple generations post-introduction. We found that mites rapidly went extinct on one-species islands, but that lizards introduced to the two-species island retained mites. After three generations, the two-species island had the highest total density and biomass of lizards, but the lowest density of the introduced species, implying that the 'invasion' had been less successful. This field-transplant study suggests that native species can be 'enemy reservoirs' that facilitate co-colonization of ectoparasites with the invasive host. Broadly, these results indicate that the presence of intact and diverse native communities may help to curb invasiveness.

Plasticity of Gene Expression and Thermal Tolerance: Implications for Climate Change Vulnerability in a Tropical Forest Lizard.

AbstractTropical ectotherms are thought to be especially vulnerable to climate change because they have evolved in temporally stable thermal environments and therefore have decreased tolerance for thermal variability. Thus, they are expected to have narrow thermal tolerance ranges, live close to their upper thermal tolerance limits, and have decreased thermal acclimation capacity. Although models often predict that tropical forest ectotherms are especially vulnerable to rapid environmental shifts, these models rarely include the potential for plasticity of relevant traits. We measured phenotypic plasticity of thermal tolerance and thermal preference as well as multitissue transcriptome plasticity in response to warmer temperatures in a species that previous work has suggested is highly vulnerable to climate warming, the Panamanian slender anole lizard (Anolis apletophallus). We found that many genes, including heat shock proteins, were differentially expressed across tissues in response to short-term warming. Under long-term warming, the voluntary thermal maxima of lizards also increased, although thermal preference exhibited only limited plasticity. Using these data, we modeled changes in the activity time of slender anoles through the end of the century under climate change and found that plasticity should delay declines in activity time by at least two decades. Our results suggest that slender anoles, and possibly other tropical ectotherms, can alter the expression of genes and phenotypes when responding to shifting environmental temperatures and that plasticity should be considered when predicting the future of organisms under a changing climate.

Species-Specific Expression of Growth-Regulatory Genes in 2 Anoles with Divergent Patterns of Sexual Size Dimorphism.

Sexual size dimorphism is widespread in nature and often develops through sexual divergence in growth trajectories. In vertebrates, the growth hormone/insulin-like growth factor (GH/IGF) network is an important regulator of growth, and components of this network are often regulated in sex-specific fashion during the development of sexual size dimorphism. However, expression of the GH/IGF network is not well characterized outside of mammalian model systems, and the extent to which species differences in sexual size dimorphism are related to differences in GH/IGF network expression is unclear. To begin bridging this gap, we compared GH/IGF network expression in liver and muscle from 2 lizard congeners, one with extreme male-biased sexual size dimorphism (brown anole, Anolis sagrei), and one that is sexually monomorphic in size (slender anole, A. apletophallus). Specifically, we tested whether GH/IGF network expression in adult slender anoles resembles the highly sex-biased expression observed in adult brown anoles or the relatively unbiased expression observed in juvenile brown anoles. We found that adults of the 2 species differed significantly in the strength of sex-biased expression for several key upstream genes in the GH/IGF network, including insulin-like growth factors 1 and 2. However, species differences in sex-biased expression were minor when comparing adult slender anoles to juvenile brown anoles. Moreover, the multivariate expression of the entire GH/IGF network (as represented by the first two principal components describing network expression) was sex-biased for the liver and muscle of adult brown anoles, but not for either tissue in juvenile brown anoles or adult slender anoles. Our work suggests that species differences in sex-biased expression of genes in the GH/IGF network (particularly in the liver) may contribute to the evolution of species differences in sexual size dimorphism.