A framework for elucidating the temperature dependence of fitness

Climate warming is predicted to cause large-scale extinctions, particularly of ectothermic species. A striking difference between tropical and temperate ectotherms is that tropical species experience a mean habitat temperature that is closer to the temperature at which fitness is maximized (T(opt)) and an upper temperature limit for survival (T(max)) that is closer to T(opt) than do temperate species. Thus, even a small increase in environmental temperature could put tropical ectotherms at high risk of extinction, whereas temperate ectotherms have a wider temperature cushion. Although this pattern is widely observed, the mechanisms that produce it are not well understood. Here we develop a mathematical framework to partition the temperature response of fitness into its components (fecundity, mortality, and development) and test model predictions with data for insects. We find that fitness declines at high temperatures because the temperature responses of fecundity and mortality act in opposite ways: fecundity decreases with temperature when temperatures exceed the optimal range, whereas mortality continues to increase. The proximity of T(opt) to T(max) depends on how the temperature response of development mediates the interaction between fecundity and mortality. When development is highly temperature sensitive, mortality exceeds reproduction only after fecundity has started to decline with temperature, which causes fitness to decline rapidly to zero when temperatures exceed T(opt). The model correctly predicts empirically observed fitness-temperature relationships in insects from different latitudes. It also suggests explanations for the widely reported phenological shifts in many ectotherms and the latitudinal differences in fitness responses.     

Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts

Seasonal acclimation and thermoregulation represent major components of complex thermal strategies by which ectotherms cope with the heterogeneity of their thermal environment. Some ectotherms possess the acclimatory capacity to shift seasonally their thermoregulatory behavior, but the frequent use of constant acclimation temperatures during experiments and the lack of information about thermal heterogeneity in the field obscures the ecological relevance of this plastic response. We examined the experimentally induced seasonal acclimation of preferred body temperatures (T(p)) in alpine newts Ichthyosaura (formerly Triturus) alpestris subjected to a gradual increase in acclimation temperature from 5°C during the winter to a constant 15°C or diel fluctuations between 10° and 20°C during the spring/summer. Both the mean and range of T(p) followed the increase in mean acclimation temperature without the influence of diel temperature fluctuations. The direction and magnitude of this acclimatory capacity has the potential to increase the time window available for thermoregulation. Although thermoregulation and thermal acclimation are often considered as separate but coadapted adjustments to thermal heterogeneity, their combined response is employed by newts to tackle seasonal variation in a thermoregulatory-challenging aquatic environment.     

Do ectotherms partition thermal resources? We still do not know

Partitioning of the niche space is a mechanism used to explain the coexistence of similar species. Ectotherms have variable body temperatures and their body temperatures influence performance and, ultimately, fitness. Therefore, many ectotherms use behavioral thermoregulation to avoid reduced capacities associated with body temperatures far from the optimal temperature for performance. Several authors have proposed that thermal niche partitioning in response to interspecific competition is a mechanism that allows the coexistence of similar species of ectotherms. We reviewed studies on thermal resource partitioning to evaluate the evidence for this hypothesis. In almost all studies, there was insufficient evidence to conclude unequivocally that thermal resource partitioning allowed species coexistence. Future studies should include sites where species are sympatric and sites where they are allopatric to rule out alternative mechanisms that cause differences in thermal traits between coexisting species. There is evidence of conservatism in the evolution of most thermal traits across a wide range of taxa, but thermal performance curves and preferred temperatures do respond to strong selection under laboratory conditions. Thus, there is potential for selection to act on thermal traits in response to interspecific competition. Nevertheless, more stringent tests of the thermal resource partitioning hypothesis are required before we can assess whether it is widespread in communities of ectotherms in nature.     

Heterothermy in two mole-rat species subjected to interacting thermoregulatory challenges

Maintaining a high and constant body temperature (T(b) ) is often viewed as a fundamental benefit of endothermy, but variation in T(b) is likely the norm rather than an exception among endotherms. Thus, attempts to elucidate which factors cause T(b) of endotherms to deviate away from the T(b) that maximizes performance are becoming more common. One approach relies on an adaptive framework of thermoregulation, used for a long time to predict variation in T(b) of ectotherms, as a starting point to make predictions about the factors that should lead to thermoregulatory variation in endotherms. Here we test the predictions that when confronted with thermoregulatory challenges endotherms should (1) become more heterothermic, (2) lower their T(b) setpoint, and/or (3) increase behavioral thermoregulation (e.g., activity levels or social thermoregulation). We exposed two species of relatively homeothermic mole-rats to two such challenges: (a) ambient temperatures (T(a)) well below the thermoneutral zone and (b) increased heat loss caused by the removal of dorsal fur. In general, our results support the adaptive framework of endothermic thermoregulation with each species conforming to some of the predictions. For example, Mashona mole-rats (Fukomys darlingi) increased heterothermy as T(a) decreased, highveld mole-rats (Cryptomys hottentotus pretoriae) displayed lower T(b) 's after shaving, and both species increased behavioral thermoregulation as T(a) decreased. This suggests that there is some merit in extending the adaptive framework to endotherms. However, none of the three predictions we tested was supported under all experimental conditions, reiterating that attempts to determine universal factors causing variation in T(b) of endotherms may prove challenging.     

Modeling energetic and theoretical costs of thermoregulatory strategy

Poikilothermic ectotherms have evolved behaviours that help them maintain or regulate their body temperature (T (b)) around a preferred or 'set point' temperature (T (set)). Thermoregulatory behaviors may range from body positioning to optimize heat gain to shuttling among preferred microhabitats to find appropriate environmental temperatures. We have modelled movement patterns between an active and non-active shuttling behaviour within a habitat (as a biased random walk) to investigate the potential cost of two thermoregulatory strategies. Generally, small-bodied ectotherms actively thermoregulate while large-bodied ectotherms may passively thermoconform to their environment. We were interested in the potential energetic cost for a large-bodied ectotherm if it were forced to actively thermoregulate rather than thermoconform. We therefore modelled movements and the resulting and comparative energetic costs in precisely maintaining a T (set) for a small-bodied versus large-bodied ectotherm to study and evaluate the thermoregulatory strategy.     

不同经度地区北草蜥的喜好体温和热耐受性

在外温动物热生理特征的进化理论中,“静态”和“易变”是两个持续争论的对立观点。热生理学特征的种内变异是检验此类假设的最有力证据。本研究比较了不同经度地区北草蜥的热环境和热生理特征,以检验“静态”和“易变”假设。东部沿海地区(宁德)的环境温度高于内陆地区(贵阳),与之相适应,沿海地区北草蜥的喜好体温也高于内陆地区。然而,两地区蜥蜴的上临界温度和下临界温度无显著差异。尽管这些热生理学特征的种群间变异趋势并不一致,但是喜好温度随环境温度变化而改变的结果符合“易变”假设的预测。此外,本研究表明蜥蜴的喜好体温存在沿经度方向的地理变异。     

Evolution of viviparity in warm-climate lizards: an experimental test of the maternal manipulation hypothesis

The maternal manipulation hypothesis for the evolution of reptilian viviparity has been claimed to apply to any situation where gravid females are able to maintain body temperatures different from those available in external nests, but empirical data that support this hypothesis are very limited. Here, we tested this hypothesis using gravid females of a warm-climate lizard, Mabuya multifasciata, by subjecting them to five thermal regimes for the whole gestation period. We found gravid females selected lower body temperatures and thermoregulated more precisely than did nongravid females. Offspring produced in different treatments differed in head size, limb length and sprint speed, but not in overall body size or mass. Variation in morphological traits of offspring was induced primarily by extreme temperatures. Sprint speed of offspring was more likely affected by the mean but not by the variance of gestation temperatures. Gravid females maintained more stable body temperatures than did nongravid females not because these temperatures resulted in the optimization of offspring phenotypes but because the range of temperatures optimal for embryonic development was relatively narrow. Our data conform to the main predictions from the maternal manipulation hypothesis that females should adjust thermoregulation during pregnancy to provide optimal thermal conditions for developing embryos and that phenotypic traits forged by maternal thermoregulation should enhance offspring fitness.     

Extending the cost-benefit model of thermoregulation: high-temperature environments

The classic cost-benefit model of ectothermic thermoregulation compares energetic costs and benefits, providing a critical framework for understanding this process (Huey and Slatkin 1976 ). It considers the case where environmental temperature (T(e)) is less than the selected temperature of the organism (T(sel)), and it predicts that, to minimize increasing energetic costs of thermoregulation as habitat thermal quality declines, thermoregulatory effort should decrease until the lizard thermoconforms. We extended this model to include the case where T(e) exceeds T(sel), and we redefine costs and benefits in terms of fitness to include effects of body temperature (T(b)) on performance and survival. Our extended model predicts that lizards will increase thermoregulatory effort as habitat thermal quality declines, gaining the fitness benefits of optimal T(b) and maximizing the net benefit of activity. Further, to offset the disproportionately high fitness costs of high T(e) compared with low T(e), we predicted that lizards would thermoregulate more effectively at high values of T(e) than at low ones. We tested our predictions on three sympatric skink species (Carlia rostralis, Carlia rubrigularis, and Carlia storri) in hot savanna woodlands and found that thermoregulatory effort increased as thermal quality declined and that lizards thermoregulated most effectively at high values of T(e).     

Thermodynamics Constrains Allometric Scaling of Optimal Development Time in Insects

Development time is a critical life-history trait that has profound effects on organism fitness and on population growth rates. For ectotherms, development time is strongly influenced by temperature and is predicted to scale with body mass to the quarter power based on 1) the ontogenetic growth model of the metabolic theory of ecology which describes a bioenergetic balance between tissue maintenance and growth given the scaling relationship between metabolism and body size, and 2) numerous studies, primarily of vertebrate endotherms, that largely support this prediction. However, few studies have investigated the allometry of development time among invertebrates, including insects. Abundant data on development of diverse insects provides an ideal opportunity to better understand the scaling of development time in this ecologically and economically important group. Insects develop more quickly at warmer temperatures until reaching a minimum development time at some optimal temperature, after which development slows. We evaluated the allometry of insect development time by compiling estimates of minimum development time and optimal developmental temperature for 361 insect species from 16 orders with body mass varying over nearly 6 orders of magnitude. Allometric scaling exponents varied with the statistical approach: standardized major axis regression supported the predicted quarter-power scaling relationship, but ordinary and phylogenetic generalized least squares did not. Regardless of the statistical approach, body size alone explained less than 28% of the variation in development time. Models that also included optimal temperature explained over 50% of the variation in development time. Warm-adapted insects developed more quickly, regardless of body size, supporting the “hotter is better” hypothesis that posits that ectotherms have a limited ability to evolutionarily compensate for the depressing effects of low temperatures on rates of biological processes. The remaining unexplained variation in development time likely reflects additional ecological and evolutionary differences among insect species.     

Reaction norms for age and size at maturity in response to temperature: a test of the compound interest hypothesis

In ectotherms, temperature induces similar developmental and evolutionary responses in body size, with larger individuals occurring or evolving in low temperature environments. Based on the occasional occurrence of opposite size clines, showing a decline in body size with increasing latitude, an interaction between generation time and growing season length was suggested to account for the patterns found. Accordingly, multivoltine species with short generation times should gain high compound interest benefits from reproducing early at high temperatures, indicating potential for extra generations, even at the expense of being smaller. This should not apply for obligatorily monovoltine populations. We explicitly test the prediction that monovoltine populations (no compound interest) should be selected for large body size to maximise adult fitness, and therefore size at maturity should respond only weakly to temperature. In two monovoltine populations (an Alpine and a Western German one) of the butterfly Lycaena hippothoe, increasing temperatures had no significant effect on pupal weight and caused a slight decrease in adult weight only. In contrast, two closely related, yet potentially multivoltine Lycaena populations showed a greater weight loss at increasing temperature (in protandrous males, but not in females) and smaller adult sizes throughout. Thus, the results do support our predictions indicating that the compound interest hypothesis may yield causal explanations for the relationship between temperature and insect size at maturity. At all temperatures, the alpine population had higher growth rates and concomitantly shorter development times (not accompanied by a reduction in size) than the other, presumably indicating local adaptations to different climates.     

Could the intrinsic rate of increase represent the fitness in terrestrial ectotherms?

The intrinsic rate of increase (r_m) has been considered as an important indicator of fitness in terrestrial ectotherms since long. It is actually an equivalent to the instantaneous growth rate of the exponential equation for describing the density-independent population growth. In terrestrial ectotherms, r_m has been demonstrated to be temperature-dependent. The temperature at which r_m was maximal, was considered to be the “optimal” temperature for fitness in Amarasekare and Savage (2012), but this definition needs further analysis. Only r_m cannot provide thorough representation of fitness. Because body size can affect the competitive abilities in many terrestrial ectotherms, both population size and body size should be considered in measuring the fitness of ectotherms. The rule of “bigger is better” requires relatively low temperature to increase in body size, whereas relatively high temperature is required for a rapid increase in population size. Thus, there is presumably a trade-off in temperature for adjusting individual body size and population size to achieve maximum fitness. We hypothesized that this temperature could be reflected by the intrinsic optimum temperature for developmental rate in the Sharpe–Schoolfield–Ikemoto model, and it led to a temperature estimate around 20 °C. However, the traditional viewpoint based on the temperature corresponding to the maximal intrinsic rate of increase provides a temperature estimate around 30 °C. This study suggests that a low temperature around 20 °C might authentically represent the optimal ambient temperature for fitness in terrestrial ectotherms. It implies that thermal biologists who are interested in the effect of temperature on the fitness in terrestrial ectotherms should pay more attention to their performance at low temperature rather than high temperature.     

Density‐Dependent Foraging and Interference Competition by Common Gartersnakes are Temperature Dependent

The ideal free distribution (IFD) predicts that optimal foragers will select foraging patches to maximize food rewards and that groups of foragers should thus be distributed between food patches in proportion to the availability of food in those patches. Because many of the underlying mechanisms of foraging are temperature dependent in ectotherms, the distribution of ectothermic foragers between food patches may similarly depend on temperature because the difference in fitness rewards between these patches may change with temperature. We tested the hypothesis that the distribution of Common Gartersnakes (Thamnophis sirtalis) between food patches can be explained by an IFD, but that conformance to an IFD weakens as temperature departs from the optimal temperature because fitness rewards, interference competition and the number of individuals foraging are highest at the optimal temperature. First, we determined the optimal temperature for foraging. Second, we examined group foraging at three temperatures and three density treatments. Search time was optimized at 27°C, handling time at 29°C and digestion time at 32°C. Gartersnakes did not match an IFD at any temperature, but their distribution did change with temperature: snakes at 20°C and at 30°C selected both food patches equally, while snakes at 25°C selected the low food patch more at low density and the high food patch more at high density. Food consumption and competition increased with temperature, and handling time decreased with temperature. Temperature therefore had a strong impact on foraging, but did not affect the IFD. Future work should examine temperature‐dependent foraging in ectotherms that are known to match an IFD.     

Quantitative genetic variation for thermal performance curves within and among natural populations of Drosophila serrata

Thermal performance curves (TPCs) provide a powerful framework for studying the evolution of continuous reaction norms and for testing hypotheses of thermal adaptation. Although featured heavily in comparative studies, the framework has been comparatively underutilized for quantitative genetic tests of thermal adaptation. We assayed the distribution of genetic (co)variance for TPC (locomotor activity) within and among three natural populations of Drosophila serrata and performed replicated tests of two hypotheses of thermal adaptation--that 'hotter is better' and that a generalist-specialist trade-off underpins the evolution of thermal sensitivity. We detected significant genetic variance within, and divergence among, populations. The 'hotter is better' hypothesis was not supported as the genetic correlations between optimal temperature (T(opt)) and maximum performance (z(max)) were consistently negative. A pattern of variation consistent with a generalist-specialist trade-off was detected within populations and divergence among populations indicated that performance curves were narrower and had higher optimal temperatures in the warmer, but less variable tropical population.     

Hypoxic metabolic response of the golden-mantled ground squirrel.

We examined the magnitude of the hypoxic metabolic response in golden-mantled ground squirrels to determine whether the shift in thermoregulatory set point (T(set)) and subsequent fall in body temperature (T(b)) and metabolic rate observed in small mammals were greater in a species that routinely experiences hypoxic burrows and hibernates. We measured the effects of changing ambient temperature (T(a); 6--29 degrees C) on metabolism (O(2) consumption and CO(2) production), T(b), ventilation, and heart rate in normoxia and hypoxia (7% O(2)). The magnitude of the hypoxia-induced falls in T(b) and metabolism of the squirrels was larger than that of other rodents. Metabolic rate was not simply suppressed but was regulated to assist the initial fall in T(b) and then acted to slow this fall and stabilize T(b) at a new, lower level. When T(a) was reduced during 7% O(2), animals were able to maintain or elevate their metabolic rates, suggesting that O(2) was not limiting. The slope of the relationship between temperature-corrected O(2) consumption and T(a) extrapolated to a T(set) in hypoxia equals the actual T(b). The data suggest that T(set) was proportionately related to T(a) in hypoxia and that there was a shift from increasing ventilation to increasing O(2) extraction as the primary strategy employed to meet increasing metabolic demands under hypoxia. The animals were neither hypothermic nor hypometabolic, as T(b) and metabolic rate appeared to be tightly regulated at new but lower levels as a result of a coordinated hypoxic metabolic response.     

Ecological constraints on the evolutionary association between field and preferred temperatures in Tropidurinae lizards

Ectothermic body temperatures affect organismal performances and presumably fitness, and are strongly influenced by the thermal environment. Therefore, the processes of colonization of novel thermal habitats by lizards might involve changes in thermal preferences, performance curves (reaction norms) and field activity temperatures. According to theory based on optimality analysis, diverse aspects of the thermal biology of vertebrate ectotherms should co-evolve as to maximize performance at the temperature range more often experienced by animals in the field. One corollary of this premise is that derived lizard clades that experienced a significant shift in thermal ecology, in comparison with the ancestral condition, should prefer and select temperatures in a thermal gradient similar to those experienced in nature. Here we report an analysis of the premise stated before. Specifically, we verify whether or not Tropidurinae species from three major Brazilian habitats (the Rainforests, the semi-arid Caatingas and the Cerrados, a Savannah-like biome) differ in thermal ecology and thermoregulatory behavior. The Caatinga is believed to be the ancestral habitat of this sub-family, and differences are expected because species from semi-arid habitats usually exhibit high body temperatures for lizards, whereas forest specialists might be thermoconformers and active at low temperatures. We also compared selected temperatures in the laboratory by species from the two open habitats (Caatingas and Cerrados). Data were analyzed using both conventional and phylogenetic analysis tools. Although species from Caatingas exhibited higher activity temperatures in nature than those from Cerrados, mean selected temperatures were similar between ecological groups. Phylogenetic analyses confirmed these findings and evidenced large␣evolutionary divergence in field activity temperatures between sister species from different␣open habitats without coupled divergence in selected temperatures. Therefore, thermoregulatory behavior and ecological parameters did not evolve similarly during the colonization of contrasting open habitats by Tropidurinae.     

Disentangling thermal preference and the thermal dependence of movement in ectotherms

Many ectotherms thermoregulate by choosing environmental temperatures that maximize diverse performance traits, including fitness. For this reason, physiological ecologists have measured preferred temperatures of diverse ectotherms for nearly a century. Thermal preference is usually measured by observing organism distributions on laboratory thermal gradients. This approach is appropriate for large ectotherms which have sufficient thermal inertia to decouple body temperatures from gradient temperatures. However, body temperatures and therefore speeds of movement of small ectotherms will closely track gradient temperature, making it difficult to distinguish between thermal preference and thermal dependence of movement. Here we develop and demonstrate the use of a patch model to derive the expected thermal gradient distribution given only the thermal dependence of movement. Comparison of this null distribution with the observed gradient distribution reveals thermal preference of small ectotherms.     

‘Optimal thermal range’ in ectotherms: Defining criteria for tests of the temperature-size-rule

Thermal performance curves for population growth rate r (a measure of fitness) were estimated over a wide range of temperature for three species: Coleps hirtus (Protista), Lecane inermis (Rotifera) and Aeolosoma hemprichi (Oligochaeta). We measured individual body size and examined if predictions for the temperature-size rule (TSR) were valid for different temperatures. All three organisms investigated follow the TSR, but only over a specific range between minimal and optimal temperatures, while maintenance at temperatures beyond this range showed the opposite pattern in these taxa. We consider minimal and optimal temperatures to be species-specific, and moreover delineate a physiological range outside of which an ectotherm is constrained against displaying size plasticity in response to temperature. This thermal range concept has important implications for general size-temperature studies. Furthermore, the concept of 'operating thermal conditions' may provide a new approach to (i) defining criteria required for investigating and interpreting temperature effects, and (ii) providing a novel interpretation for many cases in which species do not conform to the TSR.     

The mean and variance of environmental temperature interact to determine physiological tolerance and fitness

Global climate change poses one of the greatest threats to biodiversity. Most analyses of the potential biological impacts have focused on changes in mean temperature, but changes in thermal variance will also impact organisms and populations. We assessed the combined effects of the mean and variance of temperature on thermal tolerances, organismal survival, and population growth in Drosophila melanogaster. Because the performance of ectotherms relates nonlinearly to temperature, we predicted that responses to thermal variation (±0° or ±5°C) would depend on the mean temperature (17° or 24°C). Consistent with our prediction, thermal variation enhanced the rate of population growth (r(max)) at a low mean temperature but depressed this rate at a high mean temperature. The interactive effect on fitness occurred despite the fact that flies improved their heat and cold tolerances through acclimation to thermal conditions. Flies exposed to a high mean and a high variance of temperature recovered from heat coma faster and survived heat exposure better than did flies that developed at other conditions. Relatively high survival following heat exposure was associated with low survival following cold exposure. Recovery from chill coma was affected primarily by the mean temperature; flies acclimated to a low mean temperature recovered much faster than did flies acclimated to a high mean temperature. To develop more realistic predictions about the biological impacts of climate change, one must consider the interactions between the mean environmental temperature and the variance of environmental temperature.     

Climate variability slows evolutionary responses of Colias butterflies to recent climate change

How does recent climate warming and climate variability alter fitness, phenotypic selection and evolution in natural populations? We combine biophysical, demographic and evolutionary models with recent climate data to address this question for the subalpine and alpine butterfly, Colias meadii, in the southern Rocky Mountains. We focus on predicting patterns of selection and evolution for a key thermoregulatory trait, melanin (solar absorptivity) on the posterior ventral hindwings, which affects patterns of body temperature, flight activity, adult and egg survival, and reproductive success in Colias. Both mean annual summer temperatures and thermal variability within summers have increased during the past 60 years at subalpine and alpine sites. At the subalpine site, predicted directional selection on wing absorptivity has shifted from generally positive (favouring increased wing melanin) to generally negative during the past 60 years, but there is substantial variation among years in the predicted magnitude and direction of selection and the optimal absorptivity. The predicted magnitude of directional selection at the alpine site declined during the past 60 years and varies substantially among years, but selection has generally been positive at this site. Predicted evolutionary responses to mean climate warming at the subalpine site since 1980 is small, because of the variability in selection and asymmetry of the fitness function. At both sites, the predicted effects of adaptive evolution on mean population fitness are much smaller than the fluctuations in mean fitness due to climate variability among years. Our analyses suggest that variation in climate within and among years may strongly limit evolutionary responses of ectotherms to mean climate warming in these habitats.     

Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction

Adaptation in dynamic environments depends on the grain, magnitude and predictability of ecological fluctuations experienced within and across generations. Phenotypic plasticity is a well-studied mechanism in this regard, yet the potentially complex effects of stochastic environmental variation on optimal mean trait values are often overlooked. Using an optimality model inspired by timing of reproduction in great tits, we show that temporal variation affects not only optimal reaction norm slope, but also elevation. With increased environmental variation and an asymmetric relationship between fitness and breeding date, optimal timing shifts away from the side of the fitness curve with the steepest decline. In a relatively constant environment, the timing of the birds is matched with the seasonal food peak, but they become adaptively mismatched in environments with temporal variation in temperature whenever the fitness curve is asymmetric. Various processes affecting the survival of offspring and parents influence this asymmetry, which collectively determine the 'safest' strategy, i.e. whether females should breed before, on, or after the food peak in a variable environment. As climate change might affect the (co)variance of environmental variables as well as their averages, risk aversion may influence how species should shift their seasonal timing in a warming world.