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ABSTRACT Climate change can influence host–parasite dynamics by altering the abundance and distribution of hosts and their parasites as well as the physiology of both parasite and host. While the physiological effects of hosting parasites have been extensively studied in aquatic and laboratory model systems, these dynamics have been much less studied in wild terrestrial vertebrates, such as ectotherms that live in tropical forests. These organisms are particularly vulnerable to climate change because they have limited scope for behavioral buffering of stressful temperatures while already living at body temperatures close to their heat tolerance limits. Thus, it is imperative to understand how parasitism and tolerance to stressful thermal conditions, both of which are changing under climate warming, might interact to shape survival of non-model organisms. We measured heat tolerance and assessed endoparasites and ectoparasites in slender anole lizards (Anolis apletophallus; a lowland tropical forest species from central Panama). We then treated lizards with the antiparasitic drugs ivermectin and praziquantel and measured changes in immune function and heat tolerance compared with an unmanipulated control group. Immune function was not altered by treatment; however, heat tolerance increased in treated lizards. Additionally, higher endoparasite and ectoparasite abundance was associated with lower heat tolerance in a separate set of wild-caught lizards. Our results suggest that increasing environmental temperatures may have especially severe effects on host survival when parasites are present and highlight the need to consider interactions between thermal physiology and host–parasite dynamics when forecasting the responses of tropical animals to climate change. 

Synopsis Ectothermic species in lowland tropical forests have evolved in historically stable climates, leading to the prediction that transcriptomic and phenotypic plasticity do not play major roles in their responses to changes in environmental temperature. However, these species are often thermoconformers and are therefore exposed to short-term temporal fluctuations in temperature. Hence, transcriptomic plasticity in tropical forest ectotherms might replace behavioral thermoregulation as a mechanism to buffer against thermal stress. In particular, upregulation of heat shock proteins can occur during thermal stress in a range of organisms. However, while many studies have explored gene expression plasticity in response to heat stress in model organisms, little is known about transcriptomic plasticity in the tropical, non-model species that will be the most impacted by climate change. We studied the effects of moderate and severe acute heat stress events in the Panamanian slender anole (Anolis apletophallus) to gain insight into a mechanism that might allow tropical ectotherms to withstand the heat waves that are likely to rise in frequency over the coming decades under anthropogenic climate change. We found that multiple genes were upregulated across several heat shock protein networks in three tissues, and the magnitude of the expression response was similar irrespective of whether heat stress was moderate or severe. Overall, our results indicate a potentially crucial role for heat shock protein networks in the ability of tropical ectotherms to resist the negative effects of rising temperatures. 

Abstract The slender anole, Anolis apletophallus, is a small arboreal lizard of the rainforest understory of central and eastern Panama. This species has been the subject of numerous ecological and evolutionary studies over the past 60 years as a result of attributes that make it especially amenable to field and laboratory science. Slender anoles are highly abundant, short-lived (nearly 100% annual turnover), easy to manipulate in both the lab and field, and are ubiquitous in the forests surrounding the Smithsonian Tropical Research Institute in Panama, where researchers have access to high-quality laboratory facilities. Here, we present a high-quality genome for the slender anole, which is an important new resource for studying this model species. We assembled and annotated the slender anole genome by combining 3 technologies: Oxford Nanopore, 10× Genomics Linked-Reads, and Dovetail Omni-C. We compared this genome with the recently published brown anole (Anolis sagrei) and the canonical green anole (Anolis carolinensis) genomes. Our genome is the first assembled for an Anolis lizard from mainland Central or South America, the regions that host the majority of diversity in the genus. This new reference genome is one of the most complete genomes of any anole assembled to date and should facilitate deeper studies of slender anole evolution, as well as broader scale comparative genomic studies of both mainland and island species. In turn, such studies will further our understanding of the well-known adaptive radiation of Anolis lizards. 

ABSTRACT 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.