Mechanistic forecasts of species responses to climate change: The promise of biophysical ecology.

A core challenge in global change biology is to predict how species will respond to future environmental change and to manage these responses. To make such predictions and management actions robust to novel futures, we need to accurately characterize how organisms experience their environments and the biological mechanisms by which they respond. All organisms are thermodynamically connected to their environments through the exchange of heat and water at fine spatial and temporal scales and this exchange can be captured with biophysical models. Although mechanistic models based on biophysical ecology have a long history of development and application, their use in global change biology remains limited despite their enormous promise and increasingly accessible software. We contend that greater understanding and training in the theory and methods of biophysical ecology is vital to expand their application. Our review shows how biophysical models can be implemented to understand and predict climate change impacts on species' behavior, phenology, survival, distribution, and abundance. It also illustrates the types of outputs that can be generated, and the data inputs required for different implementations. Examples range from simple calculations of body temperature at a particular site and time, to more complex analyses of species' distribution limits based on projected energy and water balances, accounting for behavior and phenology. We outline challenges that currently limit the widespread application of biophysical models relating to data availability, training, and the lack of common software ecosystems. We also discuss progress and future developments that could allow these models to be applied to many species across large spatial extents and timeframes. Finally, we highlight how biophysical models are uniquely suited to solve global change biology problems that involve predicting and interpreting responses to environmental variability and extremes, multiple or shifting constraints, and novel abiotic or biotic environments.

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.

Configuration of the thermal landscape determines thermoregulatory performance of ectotherms.

Although most organisms thermoregulate behaviorally, biologists still cannot easily predict whether mobile animals will thermoregulate in natural environments. Current models fail because they ignore how the spatial distribution of thermal resources constrains thermoregulatory performance over space and time. To overcome this limitation, we modeled the spatially explicit movements of animals constrained by access to thermal resources. Our models predict that ectotherms thermoregulate more accurately when thermal resources are dispersed throughout space than when these resources are clumped. This prediction was supported by thermoregulatory behaviors of lizards in outdoor arenas with known distributions of environmental temperatures. Further, simulations showed how the spatial structure of the landscape qualitatively affects responses of animals to climate. Biologists will need spatially explicit models to predict impacts of climate change on local scales.

Recurrent sublethal warming reduces embryonic survival, inhibits juvenile growth, and alters species distribution projections under climate change.

The capacity to tolerate climate change often varies across ontogeny in organisms with complex life cycles. Recently developed species distribution models incorporate traits across life stages; however, these life-cycle models primarily evaluate effects of lethal change. Here, we examine impacts of recurrent sublethal warming on development and survival in ecological projections of climate change. We reared lizard embryos in the laboratory under temperature cycles that simulated contemporary conditions and warming scenarios. We also artificially warmed natural nests to mimic laboratory treatments. In both cases, recurrent sublethal warming decreased embryonic survival and hatchling sizes. Incorporating survivorship results into a mechanistic species distribution model reduced annual survival by up to 24% compared to models that did not incorporate sublethal warming. Contrary to models without sublethal effects, our model suggests that modest increases in developmental temperatures influence species ranges due to effects on survivorship.

Lizards perceived abiotic and biotic stressors independently when competing for shade in terrestrial mesocosms.

Hormones such as glucocorticoids and androgens enable animals to respond adaptively to environmental stressors. For this reason, circulating glucocorticoids became a popular biomarker for estimating the quality of an environment, and circulating androgens are frequently used to indicate social dominance. Here, we show that access to thermal resources influence the hormones and behavior of male lizards (Sceloporus jarrovi). We exposed isolated and paired males to different thermal landscapes, ranging from one large patch of shade to sixteen smaller patches. Both the presence of a competitor and the patchiness of the thermal environment influenced hormone concentrations and movement patterns. When shade was concentrated in space, paired lizards competed more aggressively and circulated more corticosterone. Even without competitors, lizards circulated more corticosterone in landscapes with fewer patches of shade. Conversely, shifts in circulating testosterone depended only on the relative body size of a lizard; when paired, large males and small males circulated more and less testosterone, respectively. Furthermore, isolated males moved the farthest and covered the most area when shade was concentrated in a single patch, but paired males did the opposite. Because the total area of shade in each landscape was the same, these hormonal and behavioral responses of lizards reflect the ability to access shade. Thus, circulating glucocorticoids should reflect the thermal quality of an environment when researchers have controlled for other factors. Moreover, a theory of stress during thermoregulation would help ecologists anticipate physiological and behavioral responses to changing climates.

Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs.

In recent years, ecologists have stepped up to address the challenges imposed by rapidly changing climates. Some researchers have developed niche-based methods to predict how species will shift their ranges. Such methods have evolved rapidly, resulting in models that incorporate physiological and behavioral mechanisms. Despite their sophistication, these models fail to account for environmental heterogeneity at the scale of an organism. We used an individual-based model to quantify the effects of operative environmental temperatures, as well as their heterogeneity and spatial structure, on the thermoregulation, movement, and energetics of ectotherms. Our simulations showed that the heterogeneity and spatial structure of a thermal landscape are as important as its mean temperature. In fact, temperature and heterogeneity interact to determine organismal performance. Consequently, the popular index of environmental quality (d(e)), which ignores variance and spatial structure, is inherently flawed as a descriptor of the thermal quality of an environment. Future efforts to model species' distributions should link thermoregulation and activity to environmental heterogeneity at fine scales.

Widespread rapid reductions in body size of adult salamanders in response to climate change.

Reduction in body size is a major response to climate change, yet evidence in globally imperiled amphibians is lacking. Shifts in average population body size could indicate either plasticity in the growth response to changing climates through changes in allocation and energetics, or through selection for decreased size where energy is limiting. We compared historic and contemporary size measurements in 15 Plethodon species from 102 populations (9450 individuals) and found that six species exhibited significant reductions in body size over 55 years. Biophysical models, accounting for actual changes in moisture and air temperature over that period, showed a 7.1-7.9% increase in metabolic expenditure at three latitudes but showed no change in annual duration of activity. Reduced size was greatest at southern latitudes in regions experiencing the greatest drying and warming. Our results are consistent with a plastic response of body size to climate change through reductions in body size as mediated through increased metabolism. These rapid reductions in body size over the past few decades have significance for the susceptibility of amphibians to environmental change, and relevance for whether adaptation can keep pace with climate change in the future.

Predicting the physiological performance of ectotherms in fluctuating thermal environments.

Physiological ecologists have long sought to understand the plasticity of organisms in environments that vary widely among years, seasons and even hours. This is now even more important because human-induced climate change is predicted to affect both the mean and variability of the thermal environment. Although environmental change occurs ubiquitously, relatively few researchers have studied the effects of fluctuating environments on the performance of developing organisms. Even fewer have tried to validate a framework for predicting performance in fluctuating environments. Here, we determined whether reaction norms based on performance at constant temperatures (18, 22, 26, 30 and 34°C) could be used to predict embryonic and larval performance of anurans at fluctuating temperatures (18-28°C and 18-34°C). Based on existing theory, we generated hypotheses about the effects of stress and acclimation on the predictability of performance in variable environments. Our empirical models poorly predicted the performance of striped marsh frogs (Limnodynastes peronii) at fluctuating temperatures, suggesting that extrapolation from studies conducted under artificial thermal conditions would lead to erroneous conclusions. During the majority of ontogenetic stages, growth and development in variable environments proceeded more rapidly than expected, suggesting that acute exposures to extreme temperatures enable greater performance than do chronic exposures. Consistent with theory, we predicted performance more accurately for the less variable thermal environment. Our results underscore the need to measure physiological performance under naturalistic thermal conditions when testing hypotheses about thermal plasticity or when parameterizing models of life-history evolution.

Repeatability of Voluntary Thermal Maximum and Covariance with Water Loss Reveal Potential for Adaptation to Changing Climates.

AbstractAlthough climate warming poses a grave threat to amphibians, little is known about the capacity of this group to evolve in response to warming. The capacity of key traits to evolve depends on the presence of genetic variation on which selection can act. Here, we use repeatability estimates to estimate the potential upper bounds of heritable genetic variation in voluntary and critical thermal maxima of gray-cheeked salamanders (Plethodon metcalfi). Increases in thermal tolerance may also require concordant increases in resistance to water loss because hotter temperatures incur greater evaporative risk. Therefore, we also tested for a correlation between voluntary thermal maxima and resistance to water loss and conducted an acclimation study to test for covariation between these traits in response to warming. Voluntary thermal maxima exhibited low to moderate levels of repeatability (R=0.32, P=0.045), while critical thermal maxima exhibited no statistically significant repeatability (R=0.10, P=0.57). Voluntary thermal maxima also correlated positively with resistance to water loss (R=0.31, P=0.025) but only when controlling for body mass. Voluntary thermal maxima and resistance to water loss also exhibited different acclimatory responses across control (12°C-18°C) and warm (18°C-24°C) temperature regimes, indicating a potential decoupling of traits in different thermal environments. By addressing the repeatability of thermal tolerance and the potential for covariation with resistance to water loss, we begin to address some of the key requirements of amphibians to evolve in warming climates.

Riding the wave: reconciling the roles of disease and climate change in amphibian declines.

We review the evidence for the role of climate change in triggering disease outbreaks of chytridiomycosis, an emerging infectious disease of amphibians. Both climatic anomalies and disease-related extirpations are recent phenomena, and effects of both are especially noticeable at high elevations in tropical areas, making it difficult to determine whether they are operating separately or synergistically. We compiled reports of amphibian declines from Lower Central America and Andean South America to create maps and statistical models to test our hypothesis of spatiotemporal spread of the pathogen Batrachochytrium dendrobatidis (Bd), and to update the elevational patterns of decline in frogs belonging to the genus Atelopus. We evaluated claims of climate change influencing the spread of Bd by including error into estimates of the relationship between air temperature and last year observed. Available data support the hypothesis of multiple introductions of this invasive pathogen into South America and subsequent spread along the primary Andean cordilleras. Additional analyses found no evidence to support the hypothesis that climate change has been driving outbreaks of amphibian chytridiomycosis, as has been posited in the climate-linked epidemic hypothesis. Future studies should increase retrospective surveys of museum specimens from throughout the Andes and should study the landscape genetics of Bd to map fine-scale patterns of geographic spread to identify transmission routes and processes.

A chromosome-level genome assembly for the eastern fence lizard (Sceloporus undulatus), a reptile model for physiological and evolutionary ecology.

BACKGROUND: High-quality genomic resources facilitate investigations into behavioral ecology, morphological and physiological adaptations, and the evolution of genomic architecture. Lizards in the genus Sceloporus have a long history as important ecological, evolutionary, and physiological models, making them a valuable target for the development of genomic resources. FINDINGS: We present a high-quality chromosome-level reference genome assembly, SceUnd1.0 (using 10X Genomics Chromium, HiC, and Pacific Biosciences data), and tissue/developmental stage transcriptomes for the eastern fence lizard, Sceloporus undulatus. We performed synteny analysis with other snake and lizard assemblies to identify broad patterns of chromosome evolution including the fusion of micro- and macrochromosomes. We also used this new assembly to provide improved reference-based genome assemblies for 34 additional Sceloporus species. Finally, we used RNAseq and whole-genome resequencing data to compare 3 assemblies, each representing an increased level of cost and effort: Supernova Assembly with data from 10X Genomics Chromium, HiRise Assembly that added data from HiC, and PBJelly Assembly that added data from Pacific Biosciences sequencing. We found that the Supernova Assembly contained the full genome and was a suitable reference for RNAseq and single-nucleotide polymorphism calling, but the chromosome-level scaffolds provided by the addition of HiC data allowed synteny and whole-genome association mapping analyses. The subsequent addition of PacBio data doubled the contig N50 but provided negligible gains in scaffold length. CONCLUSIONS: These new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology.

Can mechanism inform species' distribution models?

Two major approaches address the need to predict species distributions in response to environmental changes. Correlative models estimate parameters phenomenologically by relating current distributions to environmental conditions. By contrast, mechanistic models incorporate explicit relationships between environmental conditions and organismal performance, estimated independently of current distributions. Mechanistic approaches include models that translate environmental conditions into biologically relevant metrics (e.g. potential duration of activity), models that capture environmental sensitivities of survivorship and fecundity, and models that use energetics to link environmental conditions and demography. We compared how two correlative and three mechanistic models predicted the ranges of two species: a skipper butterfly (Atalopedes campestris) and a fence lizard (Sceloporus undulatus). Correlative and mechanistic models performed similarly in predicting current distributions, but mechanistic models predicted larger range shifts in response to climate change. Although mechanistic models theoretically should provide more accurate distribution predictions, there is much potential for improving their flexibility and performance.

Terrestrial Salamanders Maintain Habitat Suitability under Climate Change despite Trade-Offs between Water Loss and Gas Exchange.

Physiological acclimation has the potential to improve survival during climate change by reducing sensitivity to warming. However, acclimation can produce trade-offs due to links between related physiological traits. Water loss and gas exchange are intrinsically linked by the need for respiratory surfaces to remain moist. As climates warm and dry, organisms may attempt to lower desiccation risk by limiting water loss but at a cost of inhibiting their ability to breathe. Here we used laboratory experiments to evaluate the trade-off between water loss and gas exchange in a fully terrestrial, lungless salamander (Plethodon metcalfi). We measured acclimation of resistance to water loss and metabolic rates in response to long-term exposure to temperature and humidity treatments. We then integrated the trade-off into a simulation-based species distribution model to determine the consequences of ignoring physiological trade-offs on energy balance and aerobic scope under climate change. In the laboratory, we found a close association between acclimation of resistance to water loss and metabolic rates indicative of a trade-off. After incorporating the trade-off into our simulations, we found that energy balance and aerobic scope were reduced by 49.7% and 34.3%, respectively, under contemporary climates across their geographic range. Under future warming scenarios, incorporating the trade-off lowered the number of sites predicted to experience local extirpation by 52.2% relative to simulations without the trade-off; however, the number of sites capable of supporting the energetic requirements for reproduction declined from 44.6% to 32.6% across the species' geographic range. These experiments and simulations suggest that salamanders can maintain positive energy balance across their geographic range under climate change despite the costs associated with trade-offs between water loss and gas exchange.

Genetic variances and covariances of aerobic metabolic rates in laboratory mice.

The genetic variances and covariances of traits must be known to predict how they may respond to selection and how covariances among them might affect their evolutionary trajectories. We used the animal model to estimate the genetic variances and covariances of basal metabolic rate (BMR) and maximal metabolic rate (MMR) in a genetically heterogeneous stock of laboratory mice. Narrow-sense heritability (h(2)) was approximately 0.38 +/- 0.08 for body mass, 0.26 +/- 0.08 for whole-animal BMR, 0.24 +/- 0.07 for whole-animal MMR, 0.19 +/- 0.07 for mass-independent BMR, and 0.16 +/- 0.06 for mass-independent MMR. All h(2) estimates were significantly different from zero. The phenotypic correlation of whole animal BMR and MMR was 0.56 +/- 0.02, and the corresponding genetic correlation was 0.79 +/- 0.12. The phenotypic correlation of mass-independent BMR and MMR was 0.13 +/- 0.03, and the corresponding genetic correlation was 0.72 +/- 0.03. The genetic correlations of metabolic rates were significantly different from zero, but not significantly different from one. A key assumption of the aerobic capacity model for the evolution of endothermy is that BMR and MMR are linked. The estimated genetic correlation between BMR and MMR is consistent with that assumption, but the genetic correlation is not so high as to preclude independent evolution of BMR and MMR.

Spatial dynamics of nesting behavior: lizards shift microhabitats to construct nests with beneficial thermal properties.

Because temperature affects the growth, development, and survival of embryos, oviparous mothers should discriminate carefully among available nesting sites. We combined a radiotelemetric study of animal movements with a spatial mapping of environmental temperatures to test predictions about the nesting behavior of the eastern fence lizard (Sceloporus undulatus). Females made large excursions from their typical home ranges to construct nests in exposed substrates. These excursions appeared to be related solely to nesting because all females returned to forested habitat immediately afterward. On average, <1% (range = 0-8%, n = 19) of the area used by a female during nesting was contained within the area used before and after nesting. The selection of nesting sites matched predictions based on laboratory studies of embryonic performance; specifically, females nested in extremely open habitat at a mean of 6 cm depth. Spatial mapping of soil temperatures revealed that temperatures of nesting areas exceeded those of areas typically used by females, indicating that females preferred to construct warm nests that speed embryonic growth and development. However, this behavior could reduce the survivorship of females because of the need to rapidly navigate unfamiliar and exposed terrain.

The World Still Is Not Flat: Lessons Learned from Organismal Interactions with Environmental Heterogeneity in Terrestrial Environments.

Over the past decade, ecologists and physiologists alike have acknowledged the importance of environmental heterogeneity. Meaningful predictions of the responses of organisms to climate will require an explicit understanding of how organismal behavior and physiology are affected by such heterogeneity. Furthermore, the responses of organisms themselves are quite heterogeneous: physiology and behavior vary over different time scales and across different life stages, and because physiological systems do not operate in isolation of one another, they need to be considered in a more integrated fashion. Here, we review case studies from our laboratories to highlight progress that has been made along these fronts and generalizations that might be made to other systems, particularly in the context of predicting responses to climate change.

Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

When offspring share a womb, interactions among fetuses can impart lasting impressions on phenotypic outcomes. Such intrauterine interactions often are mediated by sex steroids (estrogens and androgens) produced by the developing fetuses. In many mammals, intrauterine interactions between brothers and sisters lead to masculinization of females, which can induce fitness consequences. Many litter-bearing primates, though, seem to escape androgen-mediated litter effects, begging why? Here, we investigated how the sex composition (i.e., same- or mixed-sex) of litters influences perinatal outcomes in the common marmoset monkey (Callithrix jacchus), using a combination of physiological, morphological, and behavioural assays. We hypothesized that androgens from male fetuses would mediate developmental differences across litter types. We found that newborns (24-36 hours old) from same- and mixed-sex litters were indistinguishable by urinary androgen profiles, birth weights, morphometrics, and behaviour. However, monkeys born into same- and mixed-sex litters exhibited subtle morphological and neurobehavioral differences later in the perinatal period, independent of their androgen profiles. Our findings suggest that while androgens from male fetuses likely do not organize their siblings' phenotypes, perinatal stimuli may initiate divergent developmental trajectories among siblings, which, in turn, promotes inter-individual variability within families.

Fundamental Flaws with the Fundamental Niche.

For more than 70 years, Hutchinson's concept of the fundamental niche has guided ecological research. Hutchinson envisioned the niche as a multidimensional hypervolume relating the fitness of an organism to relevant environmental factors. Here, we challenge the utility of the concept to modern ecologists, based on its inability to account for environmental variation and phenotypic plasticity. We have ample evidence that the frequency, duration, and sequence of abiotic stress influence the survivorship and performance of organisms. Recent work shows that organisms also respond to the spatial configuration of abiotic conditions. Spatiotemporal variation of the environment interacts with the genotype to generate a unique phenotype at each life stage. These dynamics cannot be captured adequately by a multidimensional hypervolume. Therefore, we recommend that ecologists abandon the niche as a tool for predicting the persistence of species and embrace mechanistic models of population growth that incorporate spatiotemporal dynamics.

Thermal cues drive plasticity of desiccation resistance in montane salamanders with implications for climate change.

Organisms rely upon external cues to avoid detrimental conditions during environmental change. Rapid water loss, or desiccation, is a universal threat for terrestrial plants and animals, especially under climate change, but the cues that facilitate plastic responses to avoid desiccation are unclear. We integrate acclimation experiments with gene expression analyses to identify the cues that regulate resistance to water loss at the physiological and regulatory level in a montane salamander (Plethodon metcalfi). Here we show that temperature is an important cue for developing a desiccation-resistant phenotype and might act as a reliable cue for organisms across the globe. Gene expression analyses consistently identify regulation of stem cell differentiation and embryonic development of vasculature. The temperature-sensitive blood vessel development suggests that salamanders regulate water loss through the regression and regeneration of capillary beds in the skin, indicating that tissue regeneration may be used for physiological purposes beyond replacing lost limbs.