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.

Climate anomalies and competition reduce establishment success during island colonization.

Understanding the factors that facilitate or constrain establishment of populations in novel environments is crucial for conservation biology and the study of adaptive radiation. Important questions include: (1) Does the timing of colonization relative to stochastic events, such as climatic perturbations, impact the probability of successful establishment? (2) To what extent does community context (e.g., the presence of competitors) change the probability of establishment? (3) How do sources of intrapopulation variance, such as sex differences, affect success at an individual level during the process of establishment? Answers to these questions are rarely pursued in a field-experimental context or on the same time scales (months to years) as the processes of colonization and establishment. We introduced slender anole lizards (Anolis apletophallus) to eight islands in the Panama Canal and tracked them over multiple generations to investigate the factors that mediate establishment success. All islands were warmer than the mainland (ancestral) environment, and some islands had a native competitor. We transplanted half of these populations only 4 months before the onset of a severe regional drought and the other half 2 years (two generations) before the drought. We found that successful establishment depended on both the intensity of interspecific competition and the timing of colonization relative to the drought. The islands that were colonized shortly before the drought went functionally extinct by the second generation, and regardless of time before the drought, the populations on islands with interspecific competition declined continuously over the study period. Furthermore, the effect of the competitor interacted with sex, with males suffering, and females benefitting, from the presence of a native competitor. Our results reveal that community context and the timing of colonization relative to climactic events can combine to determine establishment success and that these factors can generate opposite effects on males and females.

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.

Conservation and Management Strategies Create Opportunities for Integrative Organismal Research.

Conservation and management activities are geared toward the achievement of particular goals for a specific species, or groups of species, at the population level or higher. Conversely, organismal or functional research is typically organized by hypothesis tests or descriptive work that examines a broader theory studying individual organismal traits. Here, we outline how integrative organismal biologists might conduct mutually beneficial and meaningful research to inform or assist conservation and management biologists. We argue that studies of non-target species are very useful to both groups because non-target species can meet the goals of managers and organismal biologists alike, while also informing the other. We highlight our work on a threatened lizard species' thermal physiology, behavior, and color pattern-all of which are impacted by species management plans for sympatric, threatened, bird species. We show that management practices affect activity time, thermal adaptation, and substrate use, while also altering predation rates, crypsis, ectoparasite load, and sexual coloration in the study species. These case studies exemplify the challenges of conservation and management efforts for threatened or endangered species in that non-target species can be both positively and negatively affected by those efforts. Yet, the collaboration of organismal biologists with conservation and management efforts provides a productive system for mutually informative research.

Acclimatization in the physiological performance of an introduced ectotherm.

Phenotypic flexibility may facilitate range expansion by allowing organisms to maintain high levels of performance when introduced to novel environments. Phenotypic flexibility, such as reversible acclimatization, permits organisms to achieve high performance over a wide range of environmental conditions, without the costly allocation or acquisition tradeoffs associated with behavioral thermoregulation, which may expedite range expansion in introduced species. The northern curly-tailed lizard, Leiocephalus carinatus, was introduced to the USA in the 1940s and is now established in southern Florida. We measured bite force and the thermal sensitivity of sprinting of L. carinatus during the winter and spring to determine how morphology and performance varied seasonally. We found evidence of seasonal variation in several aspects of physiological performance. Lizards sampled in spring sprinted faster and tolerated higher temperatures, while lizards sampled in winter had high performance over a wider range of temperatures. Furthermore, seasonal differences in physiology were only detected after generating thermal reaction norms. Both sprint and bite force performance did not differ seasonally when solely comparing performance at a common temperature. No seasonal relationships between morphology and performance were detected. Our results suggest that L. carinatus may use reversible acclimatization to maintain high levels of performance across seasons not typically experienced within their native range. Thermal physiology plasticity may ameliorate the impacts of sub-optimal temperatures on performance without the cost of behavioral thermoregulation. Our work highlights the importance of utilizing reaction norms when evaluating performance and the potential ecological impacts of introduced species.

The neuroscience of adaptive thermoregulation.

The nervous system acts as a biological thermostat by controlling behaviors that regulate the warming and cooling of animals. We review the structures responsible for thermoregulation in three model species: roundworms (Caenorhabditis elegans), flies (Drosophila melanogaster), and rats (Rattus novegicus). We then consider additional features of the nervous system required to explain adaptive plasticity of the set-point temperature and the precision of thermoregulation. Because animals use resources such as energy, water, and oxygen to thermoregulate, the nervous system monitors the abundance of these resources and adjusts the strategy of thermoregulation accordingly. Starvation, dehydration, or hypoxemia alter the activity of temperature-sensitive neurons in the pre-optic area of the hypothalamus. Other regions of the brain work in conjunction with the hypothalamus to promote adaptive plasticity of thermoregulation. For example, the amygdala likely inhibits neurons of the pre-optic area, overriding thermoregulation when a risk of predation or a threat of aggression exists. Moreover, the hippocampus enables an animal to remember microhabitats that enable safe and effective thermoregulation. In ectothermic animals, such as C. elegans and D. melanogaster, the nervous system can alter set-point temperatures as the environmental temperatures change. To build on this knowledge, neuroscientists can use experimental evolution to study adaptation of neural phenotypes in controlled thermal environments. A microevolutionary perspective would leverage our understanding of ecological processes to predict the origin and maintenance of neural phenotypes by natural selection.