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AbstractThe extent to which species ranges reflect intrinsic physiological tolerances is a major question in evolutionary ecology. To date, consensus has been hindered by the limited tractability of experimental approaches across most of the tree of life. Here, we apply a macrophysiological approach to understand how hematological traits related to oxygen transport shape elevational ranges in a tropical biodiversity hot spot. Along Andean elevational gradients, we measured traits that affect blood oxygen-carrying capacity-total and cellular hemoglobin concentration and hematocrit, the volume percentage of red blood cells-for 2,355 individuals of 136 bird species. We used these data to evaluate the influence of hematological traits on elevational ranges. First, we asked whether the sensitivity of hematological traits to changes in elevation is predictive of elevational range breadth. Second, we asked whether variance in hematological traits changed as a function of distance to the nearest elevational range limit. We found that birds showing greater hematological sensitivity had broader elevational ranges, consistent with the idea that a greater acclimatization capacity facilitates elevational range expansion. We further found reduced variation in hematological traits in birds sampled near their elevational range limits and at high absolute elevations, patterns consistent with intensified natural selection, reduced effective population size, or compensatory changes in other cardiorespiratory traits. Our findings suggest that constraints on hematological sensitivity and local genetic adaptation to oxygen availability promote the evolution of the narrow elevational ranges that underpin tropical montane biodiversity.

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Macrophysiological research is vital to our understanding of mechanisms underpinning global life history variation and adaptation to diverse environments. Here, we examined latitudinal and elevational variation in a key substrate of energy metabolism and an emerging physiological component of pace-of-life syndromes, blood glucose concentration. Our data, collected from 61 European temperate and 99 Afrotropical passerine species, revealed that baseline blood glucose increases with both latitude and elevation, whereas blood glucose stress response shows divergent directions, being stronger at low latitudes and high elevations. Low baseline glucose in tropical birds, compared to their temperate counterparts, was mainly explained by their low fecundity, consistent with the slow pace-of-life syndrome in the tropics. In contrast, elevational variation in this trait was decoupled from fecundity, implying a unique montane pace-of-life syndrome combining slow-paced life histories with fast-paced physiology. The observed patterns suggest that pace-of-life syndromes do not evolve along the single fast-slow axis.

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Among ectotherms, rare species are expected to have a narrower thermal niche breadth and reduced acclimation capacity and thus be more vulnerable to global warming than their common relatives. To assess these hypotheses, we experimentally quantified the thermal sensitivity of seven common, uncommon, and rare species of temperate marine annelids of the genus Ophryotrocha to assess their vulnerability to ocean warming. We measured the upper and lower limits of physiological thermal tolerance, survival, and reproductive performance of each species along a temperature gradient (18, 24, and 30 °C). We then combined this information to produce curves of each species' fundamental thermal niche by including trait plasticity. Each thermal curve was then expressed as a habitat suitability index (HSI) and projected for the Mediterranean Sea and temperate Atlantic Ocean under a present day (1970-2000), mid- (2050-2059) and late- (2090-2099) 21st Century scenario for two climate change scenarios (RCP2.6 and RCP8.5). Rare and uncommon species showed a reduced upper thermal tolerance compared to common species, and the niche breadth and acclimation capacity were comparable among groups. The simulations predicted an overall increase in the HSI for all species and identified potential hotspots of HSI decline for uncommon and rare species along the warm boundaries of their potential distribution, though they failed to project the higher sensitivity of these species into a greater vulnerability to ocean warming. In the discussion, we provide some caveats on the implications of our results for conservation efforts.

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Thermal tolerance windows are key indicators of the range of temperatures tolerated by animals and therefore, a measure of resilience to climate change. In the ocean, where ectotherms are immersed, body temperatures are tightly coupled to environmental temperature and species have few options for thermoregulation. However, mobile species do have the ability to orientate towards optimal temperatures and move away from sub-optimal or dangerous temperatures. Escape responses are one such locomotory behavior, which typically manifests as a series of violent flicking movements that move individuals out of dangerous environments. We tested 11 species of Antarctic marine ectotherms, from one of the most stable shallow water marine environments, with an annual temperature range of -2°C to +2°C, that are vulnerable to small degrees of warming. Three species, the clam Laternula elliptica, the sea cucumber Cucumaria georgiana, and the brittlestar Ophionotus victoriae, showed no, or virtually no, escape response to temperature. Escape responses from a further eight species had a median response temperature of 11.2 (interquartile range, 10°C-15.7°C), which is well above current environmental temperatures but close to the range for acute lethal limits of Antarctic marine ectotherms (CTmax range, 17.2°C-26.6°C). This highlights that both acute tolerance limits and escape responses, fall outside current environmental temperatures, but also those predicted for 100s of years in the Southern Ocean. In a warmer Southern Ocean Antarctic fauna may not have the capacity to use temperature to select optimal thermal conditions, which leaves adaptation as a primary mechanism for their persistence.

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Physiological comparisons are fundamental to quantitative assessments of the capacity of species to persist within their current distribution and to predict their rates of redistribution in response to climate change. Yet, the degree to which physiological traits are conserved through evolutionary history may fundamentally constrain the capacity for species to adapt and shift their geographic range. Taxa that straddle major climate transitions provide the opportunity to test the mechanisms underlying evolutionary constraints and how such constraints may influence range shift predictions. Here we focus on two abundant and shallow water nacellid limpets which have representative species on either side of the Polar front. We test the thermal thresholds of the Southern Patagonian limpet, Nacella deaurata and show that its optimal temperatures for growth (4 °C), activity (-1.2 to -0.2 °C) and survival (1 to 8 °C) are mismatched to its currently experienced annual sea surface temperature range (5.9 to 10 °C). Comparisons with the congeneric Antarctic limpet, N. concinna, reveal an evolutionary constraint on N. deaurata physiology, with overlapping thermal capacities, suggesting that a cold climate legacy has been maintained through the evolution of these species. These physiological assessments predict that the South American range of N. deaurata will likely decline with continued warming. It is, however, one of the first species with demonstrated physiological capacity to successfully colonize the cold Southern Ocean. With the expected increase in opportunities for transport within high southern latitudes, N. deaurata has the potential to establish and drive ecological change within the shallow Southern Ocean.

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In lichen symbioses, fungal secondary metabolites provide UV protection on which lichen algae such as trebouxiophycean green algae-the most prominent group of photobionts in lichen symbioses-sensitively depend. These metabolites differ in their UV absorbance capability and solvability, and thus vary in their propensity of being leached from the lichen body in humid and warm environments, with still unknown implications for the global distribution of lichens. In this study covering more than 10,000 lichenised fungal species, we show that the occurrence of fungal-derived metabolites in combination with their UV absorbance capability and their probability of being leached in warm and humid environments are important eco-evolutionary drivers of global lichen distribution. Fungal-derived UV protection seems to represent an indirect environmental adaptation in which the lichen fungus invests to protect the trebouxiophycean photobiont from high UV radiation in warm and humid climates and, by doing this, secures its carbon source.

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Linking environmental conditions to the modulators of individual fitness is necessary to predict long-term population dynamics, viability, and resilience. Functional physiological, behavioral, and reproductive markers can provide this mechanistic insight into how individuals perceive physiological, psychological, chemical, and physical environmental challenges through physiological and behavioral responses that are fitness proxies. We propose a Functional Marginality framework where relative changes in allostatic load, reproductive health, and behavior can be scaled up to evidence and establish causation of macroecological processes such as local extirpation, colonization, population dynamics, and range dynamics. To fully exploit functional traits, we need to move beyond single biomarker studies to develop an integrative approach that models the interactions between extrinsic challenges, physiological, and behavioral pathways and their modulators. In addition to providing mechanistic markers of range dynamics, this approach can also serve as a valuable conservation tool for evaluating individual- and population-level health, predicting responses to future environmental change and measuring the impact of interventions. We highlight specific studies that have used complementary biomarkers to link extrinsic challenges to population performance. These frameworks of integrated biomarkers have untapped potential to identify causes of decline, predict future changes, and mitigate against future biodiversity loss.

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Thermal traits are frequently used to explain variation in species distributions, abundance, and sensitivity to climate change. Due to their utility and ease of measurement, critical thermal limits in particular have proliferated across the ecophysiological literature. Critical limit assays can, however, have deleterious or even lethal effects on individuals and there is growing recognition that intermediate metrics of performance can provide a further, nuanced understanding of how species interact with their environments. Meanwhile, the scarcity of data describing sub-critical or voluntary limits, which have been proposed as alternatives to critical limits and can be collected under less extreme conditions, reduces their value in comparative analyses and broad-scale syntheses. To overcome these limitations and determine if sub-critical limits are viable proxies for upper and lower critical thermal limits we measured and compared the critical and sub-critical thermal limits of 2023 ants representing 51 species. Sub-critical limits in isolation were a satisfactory linear predictor for both individual and species critical limits and when species identity was also considered there were substantial gains in variance explained. These gains indicate that a species-specific conversion factor can further improve estimates of critical traits using sub-critical proxies. Sub-critical limits can, therefore, be integrated into broader syntheses of critical limits and confidently used to calculate common ecological metrics, such as warming tolerance, so long as uncertainty in estimates is explicitly acknowledged. Although lower thermal traits exhibited more variation than their upper counterparts, the stronger phylogenetic signal of lower thermal traits indicates that appropriate conversions for lower thermal traits can be inferred from congenerics or other closely related taxa.

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Thermal performance traits are regularly used to make forecasts of the responses of ectotherms to anthropogenic environmental change, but such forecasts do not always differentiate between fundamental and realised thermal niches. Here we determine the relative extents to which variation in the fundamental and realised thermal niches accounts for current variation in species abundance and occupancy and assess the effects of niche-choice on future-climate response estimations. We investigated microclimate and macroclimate temperatures alongside abundance, occupancy, critical thermal limits and foraging activity of 52 ant species (accounting for >95% individuals collected) from a regional assemblage from across the Western Cape Province, South Africa, between 2003 and 2014. Capability of a species to occupy sites experiencing the most extreme temperatures, coupled with breadth of realised niche, explained most deviance in occupancy (up to 75%), while foraging temperature range and body mass explained up to 50.5% of observed variation in mean species abundance. When realised niches are used to forecast responses to climate change, large positive and negative effects among species are predicted under future conditions, in contrast to the forecasts of minimal impacts on all species that are indicated by fundamental niche predictions.

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Previous macrophysiological studies suggested that temperature-driven color lightness and body size variations strongly influence biogeographical patterns in ectotherms. However, these trait-environment relationships scale to local assemblages and the extent to which they can be modified by dispersal remains largely unexplored. We test whether the predictions of the thermal melanism hypothesis and the Bergmann's rule hold for local assemblages. We also assess whether these trait-environment relationships are more important for species adapted to less stable (lentic) habitats, due to their greater dispersal propensity compared to those adapted to stable (lotic) habitats.We quantified the color lightness and body volume of 99 European dragon- and damselflies (Odonata) and combined these trait information with survey data for 518 local assemblages across Europe. Based on this continent-wide yet spatially explicit dataset, we tested for effects temperature and precipitation on the color lightness and body volume of local assemblages and assessed differences in their relative importance and strength between lentic and lotic assemblages, while accounting for spatial and phylogenetic autocorrelation.The color lightness of assemblages of odonates increased, and body size decreased with increasing temperature. Trait-environment relationships in the average and phylogenetic predicted component were equally important for assemblages of both habitat types but were stronger in lentic assemblages when accounting for phylogenetic autocorrelation.Our results show that the mechanism underlying color lightness and body size variations scale to local assemblages, indicating their general importance. These mechanisms were of equal evolutionary significance for lentic and lotic species, but higher dispersal ability seems to enable lentic species to cope better with historical climatic changes. The documented differences between lentic and lotic assemblages also highlight the importance of integrating interactions of thermal adaptations with proxies of the dispersal ability of species into trait-based models, for improving our understanding of climate-driven biological responses.

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Thermal macrophysiology is an established research field that has led to well-described patterns in the global structuring of climate adaptation and risk. However, since it was developed primarily in animals, we lack information on how general these patterns are across organisms. This is alarming if we are to understand how thermal tolerances are distributed globally, improve predictions of climate change, and mitigate effects. We approached this knowledge gap by compiling a geographically and taxonomically extensive database on plant heat and cold tolerances and used this dataset to test for thermal macrophysiological patterns and processes in plants. We found support for several expected patterns: Cold tolerances are more variable and exhibit steeper latitudinal clines and stronger relationships with local environmental temperatures than heat tolerances overall. Next, we disentangled the importance of local environments and evolutionary and biogeographic histories in generating these patterns. We found that all three processes have significantly contributed to variation in both heat and cold tolerances but that their relative importance differs. We also show that failure to simultaneously account for all three effects overestimates the importance of the included variable, challenging previous conclusions drawn from less comprehensive models. Our results are consistent with rare evolutionary innovations in cold acclimation ability structuring plant distributions across biomes. In contrast, plant heat tolerances vary mainly as a result of biogeographical processes and drift. Our results further highlight that all plants, particularly at mid-to-high latitudes and in their nonhardened state, will become increasingly vulnerable to ongoing climate change.

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Many organisms are shrinking in size in response to global warming. However, we still lack a comprehensive understanding of the mechanisms linking body size and temperature of organisms across their geographical ranges. Here we investigate the biophysical mechanisms determining the scaling of body temperature with size across latitudes in terrestrial ectotherms. Using biophysical models, we simulated operative temperatures experienced by lizard-like ectotherms as a function of microclimatic variables, body mass and latitude and used them to generate null predictions for the effect of size on temperature across geographical gradients. We then compared model predictions against empirical data on lizards' field body temperature (Tb ) and thermal tolerance limits (CTmax and CTmin ). Our biophysical models predict that the allometric scaling of operative temperatures with body size varies with latitude, with a positive relationship at low latitudes that vanishes with increasing latitude. The analyses of thermal traits of lizards show a significant interaction of body size and latitude on Tb and CTmax and no effect of body mass on CTmin , consistent with model's predictions. The estimated scaling coefficients are within the ranges predicted by the biophysical model. The effect of body mass, however, becomes non-significant after controlling for the phylogenetic relatedness between species. We propose that large-bodied terrestrial ectotherms exhibit higher risk of overheating at low latitudes, while size differences in thermal sensitivity vanish towards higher latitudes. Our work highlights the potential of combining mechanistic models with empirical data to investigate the mechanisms underpinning broad-scale patterns and ultimately provide a null model to develop baseline expectations for further empirical research.

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Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade-off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low-latitude populations in general may be more vulnerable to predicted temperature change over the next century.

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Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

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Linking variation in species' traits to large-scale environmental gradients can lend insight into the evolutionary processes that have shaped functional diversity and future responses to environmental change. Here, we ask how heat and cold tolerance vary as a function of latitude, elevation and climate extremes, using an extensive global dataset of ectotherm and endotherm thermal tolerance limits, while accounting for methodological variation in acclimation temperature, ramping rate and duration of exposure among studies. We show that previously reported relationships between thermal limits and latitude in ectotherms are robust to variation in methods. Heat tolerance of terrestrial ectotherms declined marginally towards higher latitudes and did not vary with elevation, whereas heat tolerance of freshwater and marine ectotherms declined more steeply with latitude. By contrast, cold tolerance limits declined steeply with latitude in marine, intertidal, freshwater and terrestrial ectotherms, and towards higher elevations on land. In all realms, both upper and lower thermal tolerance limits increased with extreme daily temperature, suggesting that different experienced climate extremes across realms explain the patterns, as predicted under the Climate Extremes Hypothesis. Statistically accounting for methodological variation in acclimation temperature, ramping rate and exposure duration improved model fits, and increased slopes with extreme ambient temperature. Our results suggest that fundamentally different patterns of thermal limits found among the earth's realms may be largely explained by differences in episodic thermal extremes among realms, updating global macrophysiological 'rules'. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

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Documenting and explaining global patterns of biodiversity in time and space have fascinated and occupied biologists for centuries. Investigation of the importance of these patterns, and their underpinning mechanisms, has gained renewed vigour and importance, perhaps becoming pre-eminent, as we attempt to predict the biological impacts of global climate change. Understanding the physiological features that determine, or constrain, a species' geographical range and how they respond to a rapidly changing environment is critical. While the ecological patterns are crystallizing, explaining the role of physiology has just begun. The papers in this volume are the primary output from a Satellite Meeting of the Society of Experimental Biology Annual Meeting, held in Florence in July 2018. The involvement of two key environmental factors, temperature and oxygen, was explored through the testing of key hypotheses. The aim of the meeting was to improve our knowledge of large-scale geographical differences in physiology, e.g. metabolism, growth, size and subsequently our understanding of the role and vulnerability of those physiologies to global climate warming. While such an aim is of heuristic interest, in the midst of our current biodiversity crisis, it has an urgency that is difficult to overstate. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

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The inability of species to adapt to changing climate may cause ecological communities to disassemble and lose ecological functioning. However, theory suggests that communities may be resilient whenever populations within species exhibit variation in thermal plasticity or adaptation whereby thermally tolerant populations replace thermally sensitive ones. But will they maintain the functional roles of the populations being replaced? This study evaluated whether "like replaces like" functionally by measuring how four populations of a grasshopper herbivore and its co-occurring spider predator cope with environmental warming. The study occurred across a latitudinal gradient bounded by southerly, warmer Connecticut and northerly, cooler New Hampshire, USA. The study compared the survival rates, thermal performance, habitat usage, and food chain interactions of each grasshopper and spider population between its home field site (field of origin) and a Connecticut transplant site, and the native Connecticut population. Three grasshopper populations exhibited physiological plasticity by adjusting metabolic rates. The fourth population selected cooler habitat locations. Spider populations did not alter their metabolism and instead selected cooler habitat locations, thereby altering spatial overlap with their prey and food chain interactions. Grasshopper populations that coped physiologically consumed plants in different ratios than the fourth population and the Connecticut population. Hence, "like may not replace like" whenever populations adapt physiologically to warming.

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Geographical gradients of body size express climate-driven constraints on animals, but whether they exist and what causes them in ectotherms remains contentious. For amphibians, the water conservation hypothesis posits that larger bodies reduce evaporative water loss (EWL) along dehydrating gradients. To address this hypothesis mechanistically, we build on well-established biophysical equations of water exchange in anurans to propose a state-transition model that predicts an increase of either body size or resistance to EWL as alternative specialization along dehydrating gradients. The model predicts that species whose water economy is more sensitive to variation in body size than to variation in resistance to EWL should increase in size in response to increasing potential evapotranspiration (PET). To evaluate the model predictions, we combine physiological measurements of resistance to EWL with geographic data of body size for four different anuran species. Only one species, Dendropsophus minutus, was predicted to exhibit a positive body size-PET relationship. Results were as predicted for all cases, with one species-Boana faber-showing a negative relationship. Based on an empirically verified mathematical model, we show that clines of body size among anurans depend on the current values of those traits and emerge as an advantage for water conservation. Our model offers a mechanistic and compelling explanation for the cause and variation of gradients of body size in anurans.

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Species may exhibit similar traits via different mechanisms: environmental filtering and local adaptation (geography) and shared evolutionary history (phylogeny) can each contribute to the resemblance of traits among species. Parsing trait variation into geographic and phylogenetic sources is important, as each suggests different constraints on trait evolution. Here, we explore how phylogenetic distance, geographic distance, and geographic variation in climate shape physiological tolerance of high and low temperatures using a global dataset of ant thermal tolerances. We found generally strong roles for evolutionary history and geographic variation in temperature, but essentially no detectable effects of spatial proximity per se on either upper or lower thermal tolerance. When we compared the relative importance of the factors shaping upper and lower tolerances, we found a much stronger role for evolutionary history in shaping upper versus lower tolerance, and a moderately weaker role for geographic variation in temperature in shaping upper tolerance when compared with lower tolerance. Our results demonstrate how geographic variation in climate and evolutionary history may have differential effects on the upper and lower endpoints of physiological tolerance. This Janus effect, where the relative contributions of geographic variation in climate and evolutionary history are reversed for lower versus upper physiological tolerances, has gained some support in the literature, and our results for ant physiological tolerances provide further evidence of this pattern. As the climate continues to change, the high phylogenetic conservatism of upper tolerance may suggest potential constraints on the evolution of tolerance of high temperatures.

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Metabolic critical temperatures define the range of ambient temperatures where endotherms are able to minimize energy allocation to thermogenesis. Examining the relationship between metabolic critical temperatures and basal metabolic rates (BMR) provides a unique opportunity to gain a better understanding of how animals respond to varying ambient climatic conditions, especially in times of ongoing and projected future climate change. We make use of this opportunity by testing the heat dissipation limit (HDL) theory, which hypothesizes that the maximum amount of heat a species can dissipate constrains its energetics. Specifically, we test the theory's implicit prediction that BMR should be lower under higher metabolic critical temperatures. We analysed the relationship of BMR with upper and lower critical temperatures for a large dataset of 146 endotherm species using regression analyses, carefully accounting for phylogenetic relationships and body mass. We show that metabolic critical temperatures are negatively related with BMR in both birds and mammals. Our results confirm the predictions of the HDL theory, suggesting that metabolic critical temperatures and basal metabolic rates respond in concert to ambient climatic conditions. This implies that heat dissipation capacities of endotherms may be an important factor to take into account in assessments of species' vulnerability to climate change.