Michael J. Angilletta

Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change

Summary nThermoregulation buffers environmental variation, which enables a species to persist during climate change but ultimately hinders adaptation of thermal tolerance by weakening selective pressure. nWe used a model of optimal thermal physiology to demonstrate how thermoregulatory behaviour limits local adaptation of thermal physiology in a widespread group of lizards, the Sceloporus undulatus complex. nEmpirical data for seven populations demonstrates conservatism of thermal tolerance, consistent with the models prediction in the case of effective thermoregulation. In an eighth population, from a region where thermoregulation should be less effective, we observed greater heat tolerance and poorer cold tolerance, as predicted by our model. nBiophysical modelling indicates that lizards can avoid heat stress through thermoregulation in the coming decades but will ultimately experience an abrupt decline in the effectiveness of thermoregulation. In this scenario, thermoregulators will suffer a greater loss of performance in future climates than thermoconformers will, unless heat tolerance can evolve in a few generations. nOur analyses raises a concern that behavioural plasticity, while beneficial in the short term, will ultimately limit the physiological adaptation required to endure a warming climate.

How to avoid errors when quantifying thermal environments

Summary nModelling thermal environments at high resolution becomes simpler when using operative temperature, which condenses microclimate and morphology into an index of thermal stress. Operative temperature can be mapped using large numbers of ‘operative temperature thermometers’, hollow models that duplicate external properties of the animal. nAs climatologists predict that air will warm by 2–4xa0°C by 2100, biologists must be able to distinguish climate change from systematic errors in operative temperature of the same magnitude. nA systematic error in operative temperature of 2xa0°C or a similar amount of climate warming can change predicted surface activity and indices of habitat quality, thermoregulatory precision and predation risk by 5–12%, and in some cases more than 30%. nAs construction details of operative temperature thermometers can affect their accuracy by 2xa0°C or more, biologists should use detailed physical models calibrated against living animals over potential ranges of postures, orientations and microclimates. nWater-filled models do not measure operative temperature correctly, fail to capture thermal extremes and are an unnecessary complication as one can easily compute the body temperature of moving or stationary animals from body mass and the spatio-temporal distribution of operative temperatures.

Configuration of the thermal landscape determines thermoregulatory performance of ectotherms

Significance Environmental temperatures drive major ecological processes, largely because the physiology of any organism depends on its temperature. For this reason, many animals behave in ways that prevent their body temperatures from fluctuating, even as climate changes dramatically. Using a combination of computer simulations and controlled experiments, we show that thermoregulation depends not only on the mean and variance of operative environmental temperatures but also on the spatial arrangement of these temperatures. Our results have further implications for ecological models that rely on estimates of activity to predict the responses to climatic change. 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.

TEMPORAL VARIATION FAVORS THE EVOLUTION OF GENERALISTS IN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade‐offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments.

Resolving the life cycle alters expected impacts of climate change

Recent models predict contrasting impacts of climate change on tropical and temperate species, but these models ignore how environmental stress and organismal tolerance change during the life cycle. For example, geographical ranges and extinction risks have been inferred from thermal constraints on activity during the adult stage. Yet, most animals pass through a sessile embryonic stage before reaching adulthood, making them more susceptible to warming climates than current models would suggest. By projecting microclimates at high spatio-temporal resolution and measuring thermal tolerances of embryos, we developed a life cycle model of population dynamics for North American lizards. Our analyses show that previous models dramatically underestimate the demographic impacts of climate change. A predicted loss of fitness in 2% of the USA by 2100 became 35% when considering embryonic performance in response to hourly fluctuations in soil temperature. Most lethal events would have been overlooked if we had ignored thermal stress during embryonic development or had averaged temperatures over time. Therefore, accurate forecasts require detailed knowledge of environmental conditions and thermal tolerances throughout the life cycle.

Heat tolerance during embryonic development has not diverged among populations of a widespread species (Sceloporus undulatus)

Animals that develop in shallow soils are susceptible to lethal temperatures during heat waves. We found that developing lizards from four populations entered cardiac arrest at temperatures above 46°C. Since temperatures of natural nests can presently exceed this limit, global warming would further reduce recruitment of young.

Flies developed small bodies and small cells in warm and in thermally fluctuating environments.

SUMMARY Although plasma membranes benefit cells by regulating the flux of materials to and from the environment, these membranes cost energy to maintain. Because smaller cells provide relatively more membrane area for transport, ectotherms that develop in warm environments should consist of small cells despite the energetic cost. Effects of constant temperatures on cell size qualitatively match this prediction, but effects of thermal fluctuations on cell size are unknown. Thermal fluctuations could favour either small or large cells; small cells facilitate transport during peaks in metabolic demand whereas large cells minimize the resources needed for homeoviscous adaptation. To explore this problem, we examined effects of thermal fluctuations during development on the size of epidermal cells in the wings of Drosophila melanogaster. Flies derived from a temperate population were raised at two mean temperatures (18 and 25°C), with either no variation or a daily variation of ±4°C. Flies developed faster at a mean temperature of 25°C. Thermal fluctuations sped development, but only at 18°C. An increase in the mean and variance of temperature caused flies to develop smaller cells and wings. Thermal fluctuations reduced the size of males at 18°C and the size of females at 25°C. The thorax, the wings and the cells decreased with an increase in the mean and in the variance of temperature, but the response of cells was the strongest. Based on this pattern, we hypothesize that development of the greater area of membranes under thermal fluctuations provides a metabolic advantage that outweighs the greater energetic cost of remodelling membranes.

Indirect selection of thermal tolerance during experimental evolution of Drosophila melanogaster

Natural selection alters the distribution of a trait in a population and indirectly alters the distribution of genetically correlated traits. Long-standing models of thermal adaptation assume that trade-offs exist between fitness at different temperatures; however, experimental evolution often fails to reveal such trade-offs. Here, we show that adaptation to benign temperatures in experimental populations of Drosophila melanogaster resulted in correlated responses at the boundaries of the thermal niche. Specifically, adaptation to fluctuating temperatures (16–25°C) decreased tolerance of extreme heat. Surprisingly, flies adapted to a constant temperature of 25°C had greater cold tolerance than did flies adapted to other thermal conditions, including a constant temperature of 16°C. As our populations were never exposed to extreme temperatures during selection, divergence of thermal tolerance likely reflects indirect selection of standing genetic variation via linkage or pleiotropy. We found no relationship between heat and cold tolerances in these populations. Our results show that the thermal niche evolves by direct and indirect selection, in ways that are more complicated than assumed by theoretical models.

Oxygen supply limits the heat tolerance of lizard embryos

The mechanisms that set the thermal limits to life remain uncertain. Classically, researchers thought that heating kills by disrupting the structures of proteins or membranes, but an alternative hypothesis focuses on the demand for oxygen relative to its supply. We evaluated this alternative hypothesis by comparing the lethal temperature for lizard embryos developing at oxygen concentrations of 10–30%. Embryos exposed to normoxia and hyperoxia survived to higher temperatures than those exposed to hypoxia, suggesting that oxygen limitation sets the thermal maximum. As all animals pass through an embryonic stage where respiratory and cardiovascular systems must develop, oxygen limitation may limit the thermal niches of terrestrial animals as well as aquatic ones.

Ontogeny constrains phenology: opportunities for activity and reproduction interact to dictate potential phenologies in a changing climate.

As global warming has lengthened the active seasons of many species, we need a framework for predicting how advances in phenology shape the life history and the resulting fitness of organisms. Using an individual-based model, we show how warming differently affects annual cycles of development, growth, reproduction and activity in a group of North American lizards. Populations in cold regions can grow and reproduce more when warming lengthens their active season. However, future warming of currently warm regions advances the reproductive season but reduces the survival of embryos and juveniles. Hence, stressful temperatures during summer can offset predicted gains from extended growth seasons and select for lizards that reproduce after the warm summer months. Understanding these cascading effects of climate change may be crucial to predict shifts in the life history and demography of species.