The habitat of organisms can have a significant impact on an animal's fitness, and the ability of animals to choose suitable habitats may change with human induced global change. Urbanization in particular has had drastic effects on natural habitats including changes to the physical environment and introduction of nonnative species. Ectotherms are particularly affected by environmental changes which can impact their ability to regulate their body temperature. In this study, we compared habitat preference and the effects of habitat structure in urban and natural environments on thermal preference and thermoregulation in two species of introduced ectotherms, the brown anole, Anolis sagrei, and the bark anole, Anolis distichus. We found evidence of species- and sex-specific differences in habitat use and thermal biology related to environment (i.e. natural vs urban). The urban environment had a higher temperature and fewer available perches than the natural environment. Brown anoles were better at maintaining their preferred body temperature than bark anoles. Bark anoles occupied higher perches than brown anoles, and brown anoles exhibited a greater magnitude of sexual dimorphism in their size, habitat use, and thermal biology. The lower temperature and increased habitat space in natural environments suggests these environments are at risk of invasion by nonnative species as global warming continues, and the superior ability of brown anoles to persist and maintain their body temperatures between habitats may be a reason for their success as an invasive species across the globe.
Animals maintain close associations with diverse microbiota that inhabit their digestive tracts, and these associations can profoundly affect host physiology and fitness. Gut microbiome composition is shaped by both host traits and environmental factors, yet the relative importance of these forces remains unclear in many taxa, including squamate reptiles (lizards and snakes). To address this gap, we analysed the gut microbiomes of seven species of Anolis lizards in the lowland tropical rainforest of central Panama. We sought to determine how environmental and host species characteristics shaped gut microbiome composition. Specifically, we examined (1) interspecific variation in the anole gut microbiome, (2) the relative roles of environment and host species in shaping gut microbiomes across two study locations, and (3) patterns of phylosymbiosis. We found that host-related factors (species identity, body size, and phylogenetic distance) were significant predictors of the composition of Anolis gut microbiomes. However, environmental factors, including locality and year of sampling (associated with temperature, humidity, and precipitation), also exerted significant effects. We detected evidence of phylosymbiosis, but this pattern was moderate, possibly due to the strong effect of environmental variation. Our work contributes to the growing body of literature on lizard gut microbiomes by using comparative observations across habitats and species to identify the factors that shape these communities in the wild.
Classic theory on sex chromosome evolution predicts that selection should restore ancestral diploid expression for hemizygous X-linked genes in males. However, this dosage compensation is often incomplete, leaving the X chromosome enriched for genes with female-biased expression. In this context, iguanian lizards are noteworthy among vertebrates because several species from separate families appear to exhibit both near-complete dosage compensation and male-female expression balance across their ancient, homologous X chromosomes. We tested for similar expression balance in a phrynosomatid iguanian, Sceloporus undulatus (Eastern Fence Lizard), and instead found that both ancient and more recently sex-linked regions of the X chromosome are enriched for genes with female-biased expression, regardless of age (neonate, maturing, adult) or tissue (brain, liver, muscle). By expanding our analysis across 10 phrynosomatid species spanning 4 genera, we found that male-female expression imbalance on the ancestral region of X is phylogenetically conserved in this family. We also found that an inferred chromosomal rearrangement in S. jarrovii has resulted in the evolution of female-biased expression by a formerly autosomal region. Whereas sex-biased expression of the ancestral region of X is primarily due to females overexpressing X-linked genes relative to autosomal genes, sex-biased expression of these formerly autosomal genes in S. jarrovii is primarily due to males underexpressing genes in this putative neo-X region. We conclude that male-female expression imbalance on X is widespread across phrynosomatids, potentially reflecting both overexpression in females for ancestral regions that have evolved dosage compensation and underexpression in males for neo-X regions in which dosage compensation has yet to evolve.
Phenotypic plasticity of upper and lower thermal tolerance during parts of the annual cycle with high variation and unpredictability should theoretically be important for temperate ectotherms. However, whether thermal tolerance is plastic is unclear for most ectotherms. In addition, many ectotherms have regional heterothermy (variation in body temperature among body regions), and yet how regional heterothermy might impact plasticity of thermal tolerance is unknown. We studied the plasticity of upper thermal tolerance in response to warm temperatures in a population of the temperately distributed ring-necked snake (Diadophis punctatus) that exhibits regional heterothermy whereby head temperatures are substantially warmer than cloaca temperatures. We measured voluntary thermal maximum (VTmax, a measure of upper thermal tolerance) of ring-necked snakes, incubated ring-necked snakes at two temperatures (30 °C or 34 °C) at two durations (1 h or 3 h), and remeasured VTmax. We found that ring-necked snakes exhibited plasticity of VTmax even for short durations at relatively mild but warmer temperatures. We also found that the VTmax measured in the mouth was substantially higher than that measured in the cloaca, and that mouth VTmax was less plastic than cloacal VTmax. Together, these results suggest that at least some temperate ectotherms can exhibit plasticity of upper thermal tolerance in response to warm temperatures, and that interpretations of plasticity of VTmax depend on where temperature is measured in species with regional heterothermy. These findings have implications for understanding how variation in plasticity of thermal tolerance among body regions might impact the biological response to rapid environmental change.
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.
Anti-predator coloration is a widespread phenomenon that includes such tactics as aposematism, crypsis and mimicry. Most research on colorful anti-predator traits has focused on these well-known and well-studied tactics. One anti-predator trait that is found in diverse taxa yet is still poorly understood is anti-predator decoys. New advances in phylogenetics, genomics and molecular biology have allowed for an enriched understanding of the integrative biology of this type of anti-predator trait, particularly in lizards. While anti-predator decoy coloration is present in multiple taxa across the animal tree of life, it is particularly prevalent among lizards, which use both color and behavior to attract predator attention to the tail, which is often autotomizable and can regrow. In this Review, we discuss the integrative biology of decoy coloration in lizards, including the role of color, ontogenetic variation, gene expression and genomics. We begin by reviewing the mechanisms of the production of decoy coloration in lizards then discuss the function and macroevolution of decoy coloration. Finally, we suggest potentially fruitful avenues for future research on anti-predator decoys in lizards and other animal taxa.
Organisms often use colorful morphological traits to communicate with members of their own or other species. While “colorful signaling” systems exemplify well-known examples of the evolution of phenotypic diversity, the genetic basis of most of these traits remains unknown. Male lizards of the genus Anolis possess a colorful throat fan, or “dewlap”, that is flashed during social displays. These displays have been extensively studied in the context of their role in the adaptive radiation of the genus. In contrast, the genetic basis of the Anolis dewlap has received relatively little attention. Here, we studied the dewlap of the slender anole (Anolis apletophallus) which exhibits a dewlap polymorphism: males have either an entirely orange dewlap (“solid” morph) or a white dewlap with a basal orange spot (“bicolor” morph). To understand the inheritance of this polymorphism, we conducted 99 crosses between individuals from populations that were fixed for one morph (single/fixed/monomorphic) or contained both morphs (mixed/polymorphic). Next, we investigated the genetic architecture of this trait using a pooled population sequencing (Pool-seq) experiment. Our findings indicate that the slender anole dewlap polymorphism is best explained as an autosomal, single-locus, Mendelian trait with the solid morph allele dominant to the bicolor morph allele. Our outlier analysis of the Pool-seq data identified a region strongly associated with this trait and within this region we identified a promising candidate locus—the transcription factor single-minded 1 (SIM1)—that may underly the dewlap polymorphism.
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.
Predators with diverse diets can use generalized feeding behavior to consume different prey types or can alter behavior based upon the functional demands of each prey type. Prey choice and feeding behavior are especially important for limbless, gape-limited predators, such as snakes, because the head must capture, subdue, and ingest prey. Although previous studies have described how snakes feed on dangerous prey, these studies have not compared how behaviors might vary with different prey types. We analyzed the feeding behavior of ground snakes (Sonora episcopa) that were fed scorpions, spiders, and centipedes. Ground snakes successfully consumed each prey type using different behaviors for each prey. To capture prey, snakes used the unusual behavior of pinning prey with the ventral surface of the head with a closed mouth strike before biting. Snakes grasped and envenomated scorpions in all trials, and this behavior lasted significantly longer for scorpions than for spiders. During envenomation, snakes used their body to pin the telson of the scorpion to reduce the likelihood of being stung. Rather than using body restraint to subdue spiders, the snakes often dragged spiders across the substrate with the mandible. Scorpions repeatedly pinched and stung snakes during feeding and snakes used body restraint to subdue this prey significantly more often than spiders. Our study revealed that ground snakes alter feeding behavior based upon prey defenses and use novel prey capture and handling behaviors to subdue prey, suggesting there is yet unappreciated diversity of feeding behavior in snakes allowing them to exploit dangerous arthropod prey.
Hormones mediate sexual dimorphism by regulating sex-specific patterns of gene expression, but it is unclear how much of this regulation involves sex-specific hormone levels versus sex-specific transcriptomic responses to the same hormonal signal. Moreover, transcriptomic responses to hormones can evolve, but the extent to which hormonal pleiotropy in gene regulation is conserved across closely related species is not well understood. We addressed these issues by elevating testosterone levels in juvenile females and males of three Sceloporus lizard species before sexual divergence in circulating testosterone and then characterizing transcriptomic responses in the liver. In each species, more genes were responsive to testosterone in males than in females, suggesting that early developmental processes prime sex-specific transcriptomic responses to testosterone later in life. However, overall transcriptomic responses to testosterone were concordant between sexes, with no genes exhibiting sex-by-treatment interactions. By contrast, hundreds of genes exhibited species-by-treatment interactions, particularly when comparing distantly related species with different patterns of sexual dimorphism, suggesting evolutionary lability in gene regulation by testosterone. Collectively, our results indicate that early organizational effects may lead to sex-specific differences in the magnitude, but not the direction, of transcriptomic responses to testosterone and that the hormone-genome interface accrues regulatory changes over evolutionary time.
By allowing for increased absorption or reflectance of solar radiation, changes in pigmentation may assist ectotherms in responding to immune challenges by enabling a more precise regulation of behavioral fever or hypothermia. Variation in epigenetic characteristics may also assist in regulating immune-induced pigmentation changes and managing the body’s energetic reserves following infection. Here, we explore how dorsal pigmentation, metabolic rate, and DNA methylation in the Florida scrub lizard (Sceloporus woodi) respond to two levels of immune challenge across two habitat types. We found changes in pigmentation that are suggestive of efforts to assist in behavioral fever and hypothermia depending on the intensity of immune challenge. We also found correlations between DNA methylation in liver tissue and pigmentation change along the dorsum, indicating that color transitions may be part of a multifaceted immune response across tissue types. The relationship between immune response and metabolic rate supports the idea that energetic reserves may be conserved for the costs associated with behavioral fever when immune challenge is low and the immune functions when immune challenge is high. While immune response appeared to be unaffected by habitat type, we found differences in metabolic activity between habitats, suggesting differences in the energetic costs associated with each. To our knowledge, these results present the first potential evidence of pigmentation change in ectotherms in association with immune response. The relationship between immune response, DNA methylation, and pigmentation change also highlights the importance of epigenetic mechanisms in organism physiology.