Disentangling physiological and physical explanations for body size-dependent thermal tolerance.

The effects of climate change are often body size dependent. One contributing factor could be size-dependent thermal tolerance (SDTT), the propensity for heat and cold tolerance to vary with body size among species and among individuals within species. SDTT is hypothesized to be caused by size differences in the temperature dependence of underlying physiological processes that operate at the cellular and organ/system level (physiological SDTT). However, temperature-dependent physiology need not change with body size for SDTT to be observed. SDTT can also arise because of physical differences that affect the relative body temperature dynamics of large and small organisms (physical SDTT). In this Commentary, I outline how physical SDTT occurs, its mechanistic differences from physiological SDTT, and how physical and physiological SDTT make different predictions about organismal responses to thermal variation. I then describe how physical SDTT can influence the outcome of thermal tolerance experiments, present an experimental framework for disentangling physical and physiological SDTT, and provide examples of tests for physiological SDTT that control for physical effects using data from Anolis lizards. Finally, I discuss how physical SDTT can affect organisms in natural environments and influence their vulnerability to anthropogenic warming. Differentiating between physiological and physical SDTT is important because it has implications for how we design and interpret thermal tolerance experiments and our fundamental understanding of thermal ecology and thermal adaptation.

Habitat degradation exacerbates the effects of anthropogenic warming by removing thermal refuges.

Habitat degradation removes shaded microhabitats that serve as thermal refuges, but not all microhabitats provide equally valuable shade.

Rapid heat hardening in embryos of the lizard Anolis sagrei.

Adaptive thermal tolerance plasticity can dampen the negative effects of warming. However, our knowledge of tolerance plasticity is lacking for embryonic stages that are relatively immobile and may benefit the most from an adaptive plastic response. We tested for heat hardening capacity (a rapid increase in thermal tolerance that manifests in minutes to hours) in embryos of the lizard Anolis sagrei. We compared the survival of a lethal temperature exposure between embryos that either did (hardened) or did not (not hardened) receive a high but non-lethal temperature pre-treatment. We also measured heart rates (HRs) at common garden temperatures before and after heat exposures to assess metabolic consequences. 'Hardened' embryos had significantly greater survival after lethal heat exposure relative to 'not hardened' embryos. That said, heat pre-treatment led to a subsequent increase in embryo HR that did not occur in embryos that did not receive pre-treatment, indicative of an energetic cost of mounting the heat hardening response. Our results are not only consistent with adaptive thermal tolerance plasticity in these embryos (greater heat survival after heat exposure), but also highlight associated costs. Thermal tolerance plasticity may be an important mechanism by which embryos respond to warming that warrants greater consideration.

Trade-offs between baseline thermal tolerance and thermal tolerance plasticity are much less common than it appears.

Thermal tolerance plasticity is a core mechanism by which organisms can mitigate the effects of climate change. As a result, there is a need to understand how variation in tolerance plasticity arises. The baseline tolerance/plasticity trade-off hypothesis (hereafter referred to as the trade-off hypothesis, TOH) has recently emerged as a potentially powerful explanation. The TOH posits that organisms with high baseline thermal tolerance have reduced thermal tolerance plasticity relative to those with low baseline tolerance. Many studies have found support for the TOH. However, this support must be regarded cautiously because the most common means of testing the TOH can yield spurious "trade-offs" due to regression to the mean. I acquired data for 25 previously published analyses that supported the TOH at the intraspecific level and reanalyzed them after applying a method that adjusts plasticity estimates for regression to the mean. Only six of the 25 analyses remained statistically significant after adjustment, and effect size and variance explained decreased in all cases. The few data sets in which support for the TOH was maintained after adjustment point to areas of future study, but are too few to make generalizations at this point. In sum, regression to the mean has led to a substantial overestimation of support for the TOH and must be accounted for in future tests of the hypothesis.

Testing for genetic assimilation with phylogenetic comparative analysis: Conceptual, methodological, and statistical considerations.

Genetic assimilation is a process that leads to reduced phenotypic plasticity during adaptation to novel conditions, a potentially important phenomenon under global environmental change. Null expectations when testing for genetic assimilation, however, are not always clear. For instance, the statistical artifact of regression to the mean could bias us toward detecting genetic assimilation when it has not occurred. Likewise, the specific mechanism underlying plasticity expression may affect null expectations under neutral evolution. We used macroevolutionary numerical simulations to examine both of these important issues and their interaction, varying whether plasticity evolves, the evolutionary mechanism, trait measurement error, and experimental design. We also modified an existing reaction norm correction method to account for phylogenetic nonindependence. We found (1) regression to the mean is pervasive and can generate spurious support for genetic assimilation; (2) experimental design and post hoc correction can minimize this spurious effect; and (3) neutral evolution can produce patterns consistent with genetic assimilation without constraint or selection, depending on the mechanism of plasticity expression. Additionally, we reanalyzed published macroevolutionary data supporting genetic assimilation, and found that support was reduced after proper correction. Considerable caution is thus required whenever investigating genetic assimilation and reaction norm evolution at macroevolutionary scales.

Humanization of wildlife gut microbiota in urban environments.

Urbanization is rapidly altering Earth's environments, demanding investigation of the impacts on resident wildlife. Here, we show that urban populations of coyotes (Canis latrans), crested anole lizards (Anolis cristatellus), and white-crowned sparrows (Zonotrichia leucophrys) acquire gut microbiota constituents found in humans, including gut bacterial lineages associated with urbanization in humans. Comparisons of urban and rural wildlife and human populations revealed significant convergence of gut microbiota among urban populations relative to rural populations. All bacterial lineages overrepresented in urban wildlife relative to rural wildlife and differentially abundant between urban and rural humans were also overrepresented in urban humans relative to rural humans. Remarkably, the bacterial lineage most overrepresented in urban anoles was a Bacteroides sequence variant that was also the most significantly overrepresented in urban human populations. These results indicate parallel effects of urbanization on human and wildlife gut microbiota and suggest spillover of bacteria from humans into wildlife in cities.

Vertebrate species, such as reptiles, birds or mammals, harbour distinct communities of microbes in their digestive systems. These miniature ecosystems ­ also known as microbiomes ­ are unique to each owner and species, reflecting their diverse lifestyles and evolutionary history. Urbanisation can disrupt these delicate intestinal communities. Humans and other animals living in cities have different gut microbes to their counterparts living in rural areas. And captive species in homes and zoos often acquire human gut bacteria in their digestive systems, which can lead to health problems in these animals. So far, it has been unclear whether such a humanization of gut bacteria also affects wild animals living in and around cities. To investigate this further, Dillard et al. compared the gut microbes of wild reptiles, birds, and mammals living in close contact with humans in North America, such as coyotes, crested anole lizards and white-crowned sparrows. DNA sequencing showed that in urban environments, the composition of gut bacteria living in all three wildlife species resembled the ones in humans. The types of bacteria overrepresented in the guts of urban humans were also overrepresented in urban wildlife. This suggests that urbanization can affect the composition of gut bacteria in wildlife species by disrupting or replacing portions of their microbiome. The reason for this pattern is unclear. It is possible that humans might be sharing their gut microbes directly with city animals, or that a human-like diet is causing the change. Given the role that gut microbes play in health and disease, it is important to find out whether these changes cause the animals any harm.

Thermal Costs and Benefits of Replicated Color Evolution in the White Sands Desert Lizard Community.

AbstractTraits often contribute to multiple functions, complicating our understanding of the selective pressures that influence trait evolution. In the Chihuahuan Desert, predation is thought to be the primary driver of cryptic light coloration in three White Sands lizard species relative to the darker coloration of populations on adjacent dark soils. However, coloration also influences radiation absorption and thus animal body temperatures. We combined comparative physiological experiments and biophysical models to test for thermal consequences of evolving different color morphs in White Sands across the three species. While light and dark morphs have not evolved different physiological heat limits within species, differences in radiation absorption between morphs lead to body temperature differences that impact relative overheating risk and activity patterns. Moreover, for all three species, an idealized morph that matches the White Sands substrate would have considerably less activity time, by approximately 1 month, than existing light morphs. Overall, there are both benefits and costs to greater substrate matching, the balance of which may prevent the evolution of optimal crypsis. Our work highlights the importance of color in dictating thermal performance and the complexity inherent in understanding the evolution of coloration.

The Physiological and Evolutionary Ecology of Sperm Thermal Performance.

Ongoing anthropogenic climate change has increased attention on the ecological and evolutionary consequences of thermal variation. Most research in this field has focused on the physiology and behavior of diploid whole organisms. The thermal performance of haploid gamete stages directly tied to reproductive success has received comparatively little attention, especially in the context of the evolutionary ecology of wild (i.e., not domesticated) organisms. Here, we review evidence for the effects of temperature on sperm phenotypes, emphasizing data from wild organisms whenever possible. We find that temperature effects on sperm are pervasive, and that above normal temperatures in particular are detrimental. That said, there is evidence that sperm traits can evolve adaptively in response to temperature change, and that adaptive phenotypic plasticity in sperm traits is also possible. We place results in the context of thermal performance curves, and encourage this framework to be used as a guide for experimental design to maximize ecological relevance as well as the comparability of results across studies. We also highlight gaps in our understanding of sperm thermal performance that require attention to more fully understand thermal adaptation and the consequences of global change.

Interactions Between Temperature Variability and Reproductive Physiology Across Traits in an Intertidal Crab.

Thermal extremes alter population processes, which can result in part from temperature-induced movement at different spatial and temporal scales. Thermal thresholds for animal movement likely change based on underlying thermal physiology and life-history stage, a topic that requires greater study. The intertidal porcelain crab Petrolisthes cinctipes currently experiences temperatures that can reach near-lethal levels in the high-intertidal zone at low tide. However, the thermal thresholds that trigger migration to cooler microhabitats, and the extent to which crabs move in response to temperature, remain unknown. Moreover, the influence of reproductive status on these thresholds is rarely investigated. We integrated demographic, molecular, behavioral, and physiological measurements to determine if behavioral thermal limits varied due to reproductive state. Demographic data showed a trend for gravid, egg bearing, crabs to appear more often under rocks in the cooler intertidal zone where crab density is highest. In situ expression of 31 genes related to stress, metabolism, and growth in the field differed significantly based on intertidal elevation, with mid-intertidal crabs expressing the gene for the reproductive yolk protein vitellogenin (vg) earlier in the season. Furthermore, VG protein levels were shown to increase with density for female hemolymph. Testing for temperatures that elicit movement revealed that gravid females engage in heat avoidance behavior at lower temperatures (i.e., have a lower voluntary thermal maximum, VTmax) than non-gravid females. VTmax was positively correlated with the temperature of peak firing rate for distal afferent nerve fibers in the walking leg, a physiological relationship that could correspond to the mechanistic underpinning for temperature dependent movement. The vulnerability of marine organisms to global change is predicated by their ability to utilize and integrate physiological and behavioral strategies in response to temperature to maximize survival and reproduction. Interactions between fine-scale temperature variation and reproductive biology can have important consequences for the ecology of species, and is likely to influence how populations respond to ongoing climate change.

Culture-enriched community profiling improves resolution of the vertebrate gut microbiota.

Vertebrates harbour gut microbial communities containing hundreds of bacterial species, most of which have never been cultivated or isolated in the laboratory. The lack of cultured representatives from vertebrate gut microbiotas limits the description and experimental interrogation of these communities. Here, we show that representatives from >50% of the bacterial genera detected by culture-independent sequencing in the gut microbiotas of fence lizards, house mice, chimpanzees, and humans were recovered in mixed cultures from frozen faecal samples plated on a panel of nine media under a single growth condition. In addition, culturing captured >100 rare bacterial genera overlooked by culture-independent sequencing, more than doubling the total number of bacterial sequence variants detected. Our approach recovered representatives from 23 previously uncultured candidate bacterial genera, 12 of which were not detected by culture-independent sequencing. Results identified strategies for both indiscriminate and selective culturing of the gut microbiota that were reproducible across vertebrate species. Isolation followed by whole-genome sequencing of 161 bacterial colonies from wild chimpanzees enabled the discovery of candidate novel species closely related to the opportunistic pathogens of humans Clostridium difficile and Hungatella hathewayi. This study establishes culturing methods that improve inventories and facilitate isolation of gut microbiota constituents from a wide diversity of vertebrate species.

Heat hardening in a pair of Anolis lizards: constraints, dynamics and ecological consequences.

Heat tolerance plasticity is predicted to be an important buffer against global warming. Nonetheless, basal heat tolerance often correlates negatively with tolerance plasticity ('trade-off hypothesis'), a constraint that could limit plasticity benefits. We tested the trade-off hypothesis at the individual level with respect to heat hardening in two lizard species, Anolis carolinensis and Anolis sagrei. Heat hardening is a rapid increase in heat tolerance after heat shock that is rarely measured in reptiles but is generally considered to be a first line of physiological defense against heat. We also employed a biophysical model of operative habitat temperatures to estimate the performance consequences of hardening under ecologically relevant conditions. Anolis carolinensis hardened by 2 h post-heat shock and maintained hardening for several hours. However, A. sagrei did not harden. Biophysical models showed that hardening in A. carolinensis reduces their overheating risk in the field. Therefore, while not all lizards heat harden, hardening has benefits for species that can. We initially found a negative relationship between basal tolerance and hardening within both species, consistent with the trade-off hypothesis. However, permutation analyses showed that the apparent trade-offs could not be differentiated from statistical artifact. We found the same result when we re-analyzed published data supporting the trade-off hypothesis in another lizard species. Our results show that false positives may be common when testing the trade-off hypothesis. Statistical approaches that account for this are critical to ensure that the hypothesis, which has broad implications for thermal adaptation and responses to warming, is assessed appropriately.

Heat hardening in a pair of Anolis lizards: constraints, dynamics and ecological consequences.

Heat tolerance plasticity is predicted to be an important buffer against global warming. Nonetheless, basal heat tolerance often correlates negatively with tolerance plasticity ('trade-off hypothesis'), a constraint that could limit plasticity benefits. We tested the trade-off hypothesis at the individual level with respect to heat hardening in two lizard species, Anolis carolinensis and Anolis sagrei Heat hardening is a rapid increase in heat tolerance after heat shock that is rarely measured in reptiles but is generally considered to be a first line of physiological defense against heat. We also employed a biophysical model of operative habitat temperatures to estimate the performance consequences of hardening under ecologically relevant conditions. Anolis carolinensis hardened by 2 h post-heat shock and maintained hardening for several hours. However, A. sagrei did not harden. Biophysical models showed that hardening in A. carolinensis reduces their overheating risk in the field. Therefore, while not all lizards heat harden, hardening has benefits for species that can. We initially found a negative relationship between basal tolerance and hardening within both species, consistent with the trade-off hypothesis. However, permutation analyses showed that the apparent trade-offs could not be differentiated from statistical artifact. We found the same result when we re-analyzed published data supporting the trade-off hypothesis in another lizard species. Our results show that false positives may be common when testing the trade-off hypothesis. Statistical approaches that account for this are critical to ensure that the hypothesis, which has broad implications for thermal adaptation and responses to warming, is assessed appropriately.

Competing native and invasive Anolis lizards exhibit thermal preference plasticity in opposite directions.

Invasive species have emerged as a significant problem in the age of anthropogenic change. Behavior can be key to invasive species success and is strongly affected by temperature. Therefore, knowledge of the temperature dependence of behavior is likely critical to understand invasive species dynamics and their interactions with native species. In this study, we tested for differences in thermal preference plasticity and temperature-dependent activity levels in a pair of congeneric lizards found in the United States: the invasive Anolis sagrei and the native A. carolinensis. We predicted that A. sagrei would demonstrate greater thermal preference plasticity and would utilize a higher and/or wider range of activity temperatures than A. carolinensis. Both would point to plasticity allowing A. sagrei to behaviorally exploiting thermal conditions that A. carolinensis cannot. We found that both species exhibited plasticity in thermal preference, but in opposite directions: preferred temperatures of A. carolinensis increased with acclimation temperature, while those of A. sagrei decreased. As a result, which species had a higher thermal preference changed with acclimation conditions. We saw no difference in overall field activity rates between the species, but that A. sagrei did tend to be active over a broader range of body temperatures. In sum, we found little evidence that differences in thermal preference plasticity between the species allow A. sagrei to remain active at a higher or broader temperature range than A. carolinensis. Nonetheless, the thermal preference data suggest complementary thermal preferences between the species that could promote microclimatic partitioning, though more work is required to test this idea.

Thermal adaptation revisited: How conserved are thermal traits of reptiles and amphibians?

Ectothermic animals, such as amphibians and reptiles, are particularly sensitive to rapidly warming global temperatures. One response in these organisms may be to evolve aspects of their thermal physiology. If this response is adaptive and can occur on the appropriate time scale, it may facilitate population or species persistence in the changed environments. However, thermal physiological traits have classically been thought to evolve too slowly to keep pace with environmental change in longer-lived vertebrates. Even as empirical work of the mid-20th century offers mixed support for conservatism in thermal physiological traits, the generalization of low evolutionary potential in thermal traits is commonly invoked. Here, we revisit this hypothesis to better understand the mechanisms guiding the timing and patterns of physiological evolution. Characterizing the potential interactions among evolution, plasticity, behavior, and ontogenetic shifts in thermal physiology is critical for accurate prediction of how organisms will respond to our rapidly warming world. Recent work provides evidence that thermal physiological traits are not as evolutionarily rigid as once believed, with many examples of divergence in several aspects of thermal physiology at multiple phylogenetic scales. However, slow rates of evolution are often still observed, particularly at the warm end of the thermal performance curve. Furthermore, the context-specificity of many responses makes broad generalizations about the potential evolvability of traits tenuous. We outline potential factors and considerations that require closer scrutiny to understand and predict reptile and amphibian evolutionary responses to climate change, particularly regarding the underlying genetic architecture facilitating or limiting thermal evolution.

The Lizard Gut Microbiome Changes with Temperature and Is Associated with Heat Tolerance.

Vertebrates harbor trillions of microorganisms in the gut, collectively termed the gut microbiota, which affect a wide range of host functions. Recent experiments in lab-reared vertebrates have shown that changes in environmental temperature can induce shifts in the gut microbiota, and in some cases these shifts have been shown to affect host thermal physiology. However, there is a lack of information about the effects of temperature on the gut microbiota of wild-caught vertebrates. Moreover, in ectotherms, which are particularly vulnerable to changing temperature regimens, the extent to which microbiota composition is shaped by temperature and associated with host thermal tolerance has not been investigated. To address these issues, we monitored the gut microbiota composition of wild-caught western fence lizards (Sceloporus occidentalis) experimentally exposed to a cool-to-warm temperature transition. Comparing experimentally exposed and control lizards indicated that warm temperatures altered and destabilized the composition of the S. occidentalis gut microbiota. Warming drove a significant reduction in the relative abundances of a clade of Firmicutes, a significant increase in the rate of compositional turnover in the gut microbiota within individual lizards, and increases in the abundances of bacteria from predicted pathogenic clades. In addition, the composition of the microbiota was significantly associated with the thermal tolerance of lizards measured at the end of the experiment. These results suggest that temperature can alter the lizard gut microbiota, with potential implications for the physiological performance and fitness of natural populations.IMPORTANCE Gut microbial communities affect their animal hosts in numerous ways, motivating investigations of the factors that shape the gut microbiota and the consequences of gut microbiota variation for host traits. In this study, we tested the effects of increases in environmental temperatures on the gut microbiota of fence lizards, a vertebrate ectotherm threatened by warming climates. By monitoring lizards and their gut microbes during an experimental temperature treatment, we showed that the warming altered and destabilized the lizard gut microbiota. Moreover, measuring thermal performance of lizard hosts at the end of the experiment indicated that the composition of the gut microbiota was associated with host thermal tolerance. These results indicate that warming temperatures can alter the gut microbiota of vertebrate ectotherms and suggest relationships between variation in the gut microbiota and the thermal physiology of natural host populations.

Invasive vegetation affects amphibian skin microbiota and body condition.

Invasive plants are major drivers of habitat modification and the scale of their impact is increasing globally as anthropogenic activities facilitate their spread. In California, an invasive plant genus of great concern is Eucalyptus. Eucalyptus leaves can alter soil chemistry and negatively affect underground macro- and microbial communities. Amphibians serve as excellent models to evaluate the effect of Eucalyptus invasion on ground-dwelling species as they predate on soil arthropods and incorporate soil microbes into their microbiotas. The skin microbiota is particularly important to amphibian health, suggesting that invasive plant species could ultimately affect amphibian populations. To investigate the potential for invasive vegetation to induce changes in microbial communities, we sampled microbial communities in the soil and on the skin of local amphibians. Specifically, we compared Batrachoseps attenuatus skin microbiomes in both Eucalyptus globulus (Myrtaceae) and native Quercus agriflolia (Fagaceae) dominated forests in the San Francisco Bay Area. We determined whether changes in microbial diversity and composition in both soil and Batrachoseps attenuatus skin were associated with dominant vegetation type. To evaluate animal health across vegetation types, we compared Batrachoseps attenuatus body condition and the presence/absence of the amphibian skin pathogen Batrachochytrium dendrobatidis. We found that Eucalyptus invasion had no measurable effect on soil microbial community diversity and a relatively small effect (compared to the effect of site identity) on community structure in the microhabitats sampled. In contrast, our results show that Batrachoseps attenuatus skin microbiota diversity was greater in Quercus dominated habitats. One amplicon sequence variant identified in the family Chlamydiaceae was observed in higher relative abundance among salamanders sampled in Eucalyptus dominated habitats. We also observed that Batrachoseps attenuatus body condition was higher in Quercus dominated habitats. Incidence of Batrachochytrium dendrobatidis across all individuals was very low (only one Batrachochytrium dendrobatidis positive individual). The effect on body condition demonstrates that although Eucalyptus may not always decrease amphibian abundance or diversity, it can potentially have cryptic negative effects. Our findings prompt further work to determine the mechanisms that lead to changes in the health and microbiome of native species post-plant invasion.

Egg incubation temperature does not influence adult heat tolerance in the lizard Anolis sagrei.

Extreme heat events are becoming more common as a result of anthropogenic global change. Developmental plasticity in physiological thermal limits could help mitigate the consequences of thermal extremes, but data on the effects of early temperature exposure on thermal limits later in life are rare, especially for vertebrate ectotherms. We conducted an experiment that to our knowledge is the first to isolate the effect of egg (i.e. embryonic) thermal conditions on adult heat tolerance in a reptile. Eggs of the lizard Anolis sagrei were incubated under one of three fluctuating thermal regimes that mimicked natural nest environments and differed in mean and maximum temperatures. After emergence, all hatchlings were raised under common garden conditions until reproductive maturity, at which point heat tolerance was measured. Egg mortality was highest in the warmest treatment, and hatchlings from the warmest treatment tended to have greater mortality than those from the cooler treatments. Despite evidence that incubation temperatures were stressful, we found no evidence that incubation treatment influenced adult heat tolerance. Our results are consistent with a low capacity for organisms to increase their physiological heat tolerance via plasticity, and emphasize the importance of behavioural and evolutionary processes as mechanisms of resilience to extreme heat.

Visual "playback" of colorful signals in the field supports sensory drive for signal detectability.

Colorful visual signals are important systems for investigating the effects of signaling environments and receiver physiology on signal evolution as predicted by the sensory drive hypothesis. Support for the sensory drive hypothesis on color signal evolution is mostly based on documenting correlations between the properties of signals and habitat conditions under which the signals are given (i.e., a correlational approach) and less commonly on the use of mathematical models that integrate representations of visual environments, signal properties, and sensory systems (i.e., a functional approach). Here, we used an experimental approach in the field to evaluate signal efficacy of colorful lizard throat fans called dewlaps that show geographic variation in the lizard Anolis cristatellus. We used a remote controlled apparatus to display "fake dewlaps" to wild lizards to test for adaptive divergence in dewlap brightness (i.e., perceived intensity) among populations in situ. We found evidence of local adaptation in dewlap brightness consistent with the sensory drive hypothesis. Specifically, dewlaps that had the brightness characteristics of local lizards were more likely to be detected than those with the brightness characteristics of non-local lizards. Our findings indicate that simplified mathematical representations of visual environments may allow robust estimates of relative detectability or conspicuousness in natural habitats. We have shown the feasibility of evaluating color signal efficacy experimentally under natural conditions and demonstrate the potential advantages of presenting isolated components of signals to an intended receiver to measure their contribution to signal function.

Thermal niche evolution across replicated Anolis lizard adaptive radiations.

Elucidating how ecological and evolutionary mechanisms interact to produce and maintain biodiversity is a fundamental problem in evolutionary ecology. Here, we focus on how physiological evolution affects performance and species coexistence along the thermal niche axis in replicated radiations of Anolis lizards best known for resource partitioning based on morphological divergence. We find repeated divergence in thermal physiology within these radiations, and that this divergence significantly affects performance within natural thermal environments. Morphologically similar species that co-occur invariably differ in their thermal physiology, providing evidence that physiological divergence facilitates species coexistence within anole communities. Despite repeated divergence, phylogenetic comparative analyses indicate that physiological traits have evolved more slowly than key morphological traits related to the structural niche. Phylogenetic analyses also reveal that physiological divergence is correlated with divergence in broad-scale habitat climatic features commonly used to estimate thermal niche evolution, but that the latter incompletely predicts variation in the former. We provide comprehensive evidence for repeated adaptive evolution of physiological divergence within Anolis adaptive radiations, including the complementary roles of physiological and morphological divergence in promoting community-level diversity. We recommend greater integration of performance-based traits into analyses of climatic niche evolution, as they facilitate a more complete understanding of the phenotypic and ecological consequences of climatic divergence.

Species as Stressors: Heterospecific Interactions and the Cellular Stress Response under Global Change.

SYNOPSIS: Anthropogenic global change is predicted to increase the physiological stress of organisms through changes in abiotic conditions such as temperature, pH, and pollution. However, organisms can also experience physiological stress through interactions with other species, especially parasites, predators, and competitors. The stress of species interactions could be an important driver of species' responses to global change as the composition of biological communities change through factors such as distributional and phenological shifts. Interactions between biotic and abiotic stressors could also induce non-linear physiological stress responses under global change. One of the primary means by which organisms deal with physiological stress is through the cellular stress response (CSR), which is broadly the upregulation of a conserved set of genes that facilitate the removal and repair of damaged macromolecules. Here, we present data on behavioral interactions and CSR gene expression for two competing species of intertidal zone porcelain crab (Petrolisthes cinctipes and Petrolisthes manimaculis). We found that P. cinctipes and P. manimaculis engage in more agonistic behaviors when interacting with heterospecifics than conspecifics; however, we found no evidence that heterospecific interactions induced a CSR in these species. In addition to our new data, we review the literature with respect to CSR induction via species interactions, focusing on predator-prey systems and heterospecific competition. We find extensive evidence for predators to induce cellular stress and aspects of the CSR in prey, even in the absence of direct physical contact between species. Effects of heterospecific competition on the CSR have been studied far less, but we do find evidence that agonistic interactions with heterospecifics can induce components of the CSR. Across all published studies, there is clear evidence that species interactions can lead to cellular stress and induction of the CSR. Nonetheless, our understanding of species-induced cellular stress lags far behind our understanding of abiotic cellular stress.