The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

Is there a trade-off between peak performance and performance breadth across temperatures for aerobic scope in teleost fishes?

The physiology and behaviour of ectotherms are strongly influenced by environmental temperature. A general hypothesis is that for performance traits, such as those related to growth, metabolism or locomotion, species face a trade-off between being a thermal specialist or a thermal generalist, implying a negative correlation between peak performance and performance breadth across a range of temperatures. Focusing on teleost fishes, we performed a phylogenetically informed comparative analysis of the relationship between performance peak and breadth for aerobic scope (AS), which represents whole-animal capacity available to carry out simultaneous oxygen-demanding processes (e.g. growth, locomotion, reproduction) above maintenance. Literature data for 28 species indicate that peak aerobic capacity is not linked to thermal performance breadth and that other physiological factors affecting thermal tolerance may prevent such a trade-off from emerging. The results therefore suggest that functional links between peak and thermal breadth for AS may not constrain evolutionary responses to environmental changes such as climate warming.     

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real‐time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.     

Basking behavior predicts the evolution of heat tolerance in Australian rainforest lizards

There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming. We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks, with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms’ vulnerability and potential resilience to climate change.     

THE EVOLUTION OF ENVIRONMENTAL TOLERANCE AND RANGE SIZE: A COMPARISON OF GEOGRAPHICALLY RESTRICTED AND WIDESPREAD MIMULUS

The geographic ranges of closely related species can vary dramatically, yet we do not fully grasp the mechanisms underlying such variation. The niche breadth hypothesis posits that species that have evolved broad environmental tolerances can achieve larger geographic ranges than species with narrow environmental tolerances. In turn, plasticity and genetic variation in ecologically important traits and adaptation to environmentally variable areas can facilitate the evolution of broad environmental tolerance. We used five pairs of western North American monkeyflowers to experimentally test these ideas by quantifying performance across eight temperature regimes. In four species pairs, species with broader thermal tolerances had larger geographic ranges, supporting the niche breadth hypothesis. As predicted, species with broader thermal tolerances also had more within‐population genetic variation in thermal reaction norms and experienced greater thermal variation across their geographic ranges than species with narrow thermal tolerances. Species with narrow thermal tolerance may be particularly vulnerable to changing climatic conditions due to lack of plasticity and insufficient genetic variation to respond to novel selection pressures. Conversely, species experiencing high variation in temperature across their ranges may be buffered against extinction due to climatic changes because they have evolved tolerance to a broad range of temperatures.     

Both life‐history plasticity and local adaptation will shape range‐wide responses to climate warming in the tundra plant Silene acaulis

Many predictions of how climate change will impact biodiversity have focused on range shifts using species‐wide climate tolerances, an approach that ignores the demographic mechanisms that enable species to attain broad geographic distributions. But these mechanisms matter, as responses to climate change could fundamentally differ depending on the contributions of life‐history plasticity vs. local adaptation to species‐wide climate tolerances. In particular, if local adaptation to climate is strong, populations across a species’ range—not only those at the trailing range edge—could decline sharply with global climate change. Indeed, faster rates of climate change in many high latitude regions could combine with local adaptation to generate sharper declines well away from trailing edges. Combining 15 years of demographic data from field populations across North America with growth chamber warming experiments, we show that growth and survival in a widespread tundra plant show compensatory responses to warming throughout the species’ latitudinal range, buffering overall performance across a range of temperatures. However, populations also differ in their temperature responses, consistent with adaptation to local climate, especially growing season temperature. In particular, warming begins to negatively impact plant growth at cooler temperatures for plants from colder, northern populations than for those from warmer, southern populations, both in the field and in growth chambers. Furthermore, the individuals and maternal families with the fastest growth also have the lowest water use efficiency at all temperatures, suggesting that a trade‐off between growth and water use efficiency could further constrain responses to forecasted warming and drying. Taken together, these results suggest that populations throughout species’ ranges could be at risk of decline with continued climate change, and that the focus on trailing edge populations risks overlooking the largest potential impacts of climate change on species’ abundance and distribution.     

Altitudinal variation in egg retention and rates of embryonic development in oviparous Zootoca vivipara fits predictions from the cold-climate model on the evolution of viviparity

The evolution of reptilian viviparity is favoured, according to the cold‐climate hypothesis, at high latitudes or altitudes, where egg retention would entail thermal benefits for embryogenesis because of maternal thermoregulation. According to this hypothesis, and considering that viviparity would have evolved through a gradual increase in the extent of intrauterine egg retention, highland oviparous populations are expected to exhibit more advanced embryo development at oviposition than lowland populations. We tested for possible differences in the level of egg retention, embryo development time and thermal biology of oviparous Zootoca vivipara near the extreme altitudinal limits of the species distribution in the north of Spain (mean altitude for lowland populations, 235 m asl.; for highland populations, 1895 m asl.). Altitude influenced neither temperature of active lizards in the field nor temperature selected by lizards in a laboratory thermal gradient, and pregnant females selected lower temperatures in the thermal gradient than did males and nonpregnant females across altitudinal levels. Eggs from highland populations contained embryos more developed at the time of oviposition (Dufaure and Hubert's stages 33–35) than eggs of highland populations (stages 30–34) and partly because of this difference incubation time was shorter for highland embryos. When analysed for clutches from both altitudinal extremes at the same embryonic stage at oviposition (stage 33), again incubation time was shorter for highland populations, indicating genuine countergradient variation in developmental rate. Our results indicate that temperature is an environmental factor affecting the geographical distribution of different levels of egg retention in Z. vivipara, as predicted by the cold‐climate hypothesis on the evolution of viviparity.     

Temperature‐related geographical shifts among passerines: contrasting processes along poleward and equatorward range margins

Climate change is causing widespread geographical range shifts, which likely reflects different processes at leading and trailing range margins. Progressive warming is thought to relax thermal barriers at poleward range margins, enabling colonization of novel areas, but imposes increasingly unsuitable thermal conditions at equatorward margins, leading to range losses from those areas. Few tests of this process during recent climate change have been possible, but understanding determinants of species’ range limits will improve predictions of their geographical responses to climate change and variation in extinction risk. Here, we examine the relationship between poleward and equatorward range margin dynamics with respect to temperature‐related geographical limits observed for 34 breeding passerine species in North America between 1984–1988 and 2002–2006. We find that species’ equatorward range margins were closer to their upper realized thermal niche limits and proximity to those limits predicts equatorward population extinction risk through time. Conversely, the difference between breeding bird species’ poleward range margin temperatures and the coolest temperatures they tolerate elsewhere in their ranges was substantial and remained consistent through time: range expansion at species’ poleward range margins is unlikely to directly reflect lowered thermal barriers to colonization. The process of range expansion may reflect more complex factors operating across broader areas of species’ ranges. The latitudinal extent of breeding bird ranges is decreasing through time. Disparate responses observed at poleward versus equatorward margins arise due to differences in range margin placement within the realized thermal niche and suggest that climate‐induced geographical shift at equatorward range limits more strongly reflect abiotic conditions than at their poleward range limits. This further suggests that observed geographic responses to date may fail to demonstrate the true cost of climate change on the poleward portion of species’ distributions. Poleward range margins for North American breeding passerines are not presently in equilibrium with realized thermal limits.     

Local thermal adaptation and local temperature regimes drive the performance of a parasitic helminth under climate change: The case of Marshallagia marshalli from wild ungulates

Across a species' range, populations are exposed to their local thermal environments, which on an evolutionary scale, may cause adaptative differences among populations. Helminths often have broad geographic ranges and temperature-sensitive life stages but little is known about whether and how local thermal adaptation can influence their response to climate change. We studied the thermal responses of the free-living stages of Marshallagia marshalli, a parasitic nematode of wild ungulates, along a latitudinal gradient. We first determine its distribution in wild sheep species in North America. Then we cultured M. marshalli eggs from different locations at temperatures from 5 to 38°C. We fit performance curves based on the metabolic theory of ecology to determine whether development and mortality showed evidence of local thermal adaptation. We used parameter estimates in life-cycle-based host–parasite models to understand how local thermal responses may influence parasite performance under general and location-specific climate-change projections. We found that M. marshalli has a wide latitudinal and host range, infecting wild sheep species from New Mexico to Yukon. Increases in mortality and development time at higher temperatures were most evident for isolates from northern locations. Accounting for location-specific parasite parameters primarily influenced the magnitude of climate change parasite performance, while accounting for location-specific climates primarily influenced the phenology of parasite performance. Despite differences in development and mortality among M. marshalli populations, when using site-specific climate change projections, there was a similar magnitude of impact on the relative performance of M. marshalli among populations. Climate change is predicted to decrease the expected lifetime reproductive output of M. marshalli in all populations while delaying its seasonal peak by approximately 1 month. Our research suggests that accurate projections of the impacts of climate change on broadly distributed species need to consider local adaptations of organisms together with local temperature profiles and climate projections.     

The legacy of past climate and landscape change on species' current experienced climate and elevation ranges across latitude: a multispecies study utilizing mammals in western North America

Aim Elevation and climate ranges across latitude experienced by 21 wide‐ranging mammal species in western North America were summarized to examine two questions: (1) do populations in the northern and southern portions of a species’ range experience different climates or are environments selected to remain similar to climates at the core of ranges; and (2) how do species’ elevational ranges, experienced temperature seasonality and temperature ranges change across latitude? Given the larger effects of climate oscillations in the north vs. the south, a predicted outcome is for species to conserve climate niches across latitude and to show reduced climate and elevation ranges in the north. An alternative outcome is latitudinal niche diversification and increased climate variation in the north. Location Western North America. Methods The questions above were examined using a combination of species occurrence data bases, climate data bases, simple summaries of means and standard deviations and by testing summaries against random distributions across latitude for 21 mammal species from a variety of orders. Results The results showed that: (i) most species conserve their niche strongly or weakly given overall temperature gradients from north to south; (ii) seasonality experienced by species is relatively static until the highest latitudes despite directional trends across the region; and (iii) the elevation range and temperature variation that species experience decreases from south to north. Main conclusions Populations at range edges appear to partition environments to remain closer to temperature values similar to those at the core of the range. In addition, seasonality is not a likely explanatory factor of genetic diversity in latitudinal gradients. The data are instead more consistent with predictions that a combination of higher gene‐flow, increasing environmental instability and decreasing elevation gradients in the north compared to the south may lead to negative correlations between latitude and species’ climate variation. The results corroborate risks faced by northern mammal populations to global climate changes.     

Variation in growth and developmental responses to supraoptimal temperatures near latitudinal range limits of gypsy moth Lymantria dispar (L.), an expanding invasive species

Variation in thermal performance within and between populations provides the potential for adaptive responses to increasing temperatures associated with climate change. Organisms experiencing temperatures above their optimum on a thermal performance curve exhibit rapid declines in function and these supraoptimal temperatures can be a critical physiological component of range limits. The gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae), is one of the best‐documented biological invasions and factors driving its spatial spread are of significant ecological and economic interest. The present study examines gypsy moth sourced from different latitudes across its North American range for sensitivity to high temperature in constant temperature growth chamber experiments. Supraoptimal temperatures result in higher mortality in northern populations compared with populations from the southern range extent (West Virginia and coastal plain of Virginia, U.S.A.). Sublethal effects of high temperature on traits associated with fitness, such as smaller pupal mass, are apparent in northern and West Virginia populations. Overall, the results indicate that populations near the southern limits of the range are less sensitive to high temperatures than northern populations from the established range. However, southern populations are lower performing overall, based on pupal mass and development time, relative to northern populations. This suggests that there may be a trade‐off associated with decreased heat sensitivity in gypsy moth. Understanding how species adapt to thermal limits and possible fitness trade‐offs of heat tolerance represents an important step toward predicting climatically driven changes in species ranges, which is a particularly critical consideration in conservation and invasion ecology.     

Thermal plasticity in postembryonic life history traits of a widely distributed Collembola: Effects of macroclimate and microhabitat on genotypic differences

Life history traits in many ectotherms show complex patterns of variation among conspecific populations sampled along wide latitudinal or climatic gradients. However, few studies have assessed whether these patterns can be explained better by thermal reaction norms of multiple life history traits, covering major aspects of the life cycle. In this study, we compared five populations of a Holarctic, numerically dominant soil microarthropod species, Folsomia quadrioculata, sampled from a wide latitudinal gradient (56–81°N), for growth, development, fecundity, and survival across four temperatures (10, 15, 20, and 25°C) in common garden experiments. We evaluated the extent to which macroclimate could explain differences in thermal adaptation and life history strategies among populations. The common garden experiments revealed large genotypic differences among populations in all the traits, which were little explained by latitude and macroclimate. In addition, the life history strategies (traits combined) hardly revealed any systematic difference related to latitude and macroclimate. The overall performance of the northernmost population from the most stochastic microclimate and the southernmost population, which remains active throughout the year, was least sensitive to the temperature treatments. In contrast, performance of the population from the most predictable microclimate peaked within a narrow temperature range (around 15°C). Our findings revealed limited support for macroclimate‐based predictions, and indicated that local soil habitat conditions related to predictability and seasonality might have considerable influence on the evolution of life history strategies of F. quadrioculata. This study highlights the need to combine knowledge on microhabitat characteristics, and demography, with findings from common garden experiments, for identifying the key drivers of life history evolution across large spatial scales, and wide climate gradients. We believe that similar approaches may substantially improve the understanding of adaptation in many terrestrial ectotherms with low dispersal ability.     

The shape of abundance distributions across temperature gradients in reef fishes

Improving predictions of ecological responses to climate change requires understanding how local abundance relates to temperature gradients, yet many factors influence local abundance in wild populations. We evaluated the shape of thermal‐abundance distributions using 98 422 abundance estimates of 702 reef fish species worldwide. We found that curved ceilings in local abundance related to sea temperatures for most species, where local abundance declined from realised thermal ‘optima’ towards warmer and cooler environments. Although generally supporting the abundant‐centre hypothesis, many species also displayed asymmetrical thermal‐abundance distributions. For many tropical species, abundances did not decline at warm distribution edges due to an unavailability of warmer environments at the equator. Habitat transitions from coral to macroalgal dominance in subtropical zones also influenced abundance distribution shapes. By quantifying the factors constraining species’ abundance, we provide an important empirical basis for improving predictions of community re‐structuring in a warmer world.     

Thermal tolerance and geographical range size in the Agabus brunneus group of European diving beetles (Coleoptera: Dytiscidae)

Aim Within clades, most taxa are rare, whilst few are common, a general pattern for which the causes remain poorly understood. Here we investigate the relationship between thermal performance (tolerance and acclimation ability) and the size of a species’ geographical range for an assemblage of four ecologically similar European diving beetles (the Agabus brunneus group) to examine whether thermal physiology relates to latitudinal range extent, and whether Brown’s hypothesis and the environmental variability hypothesis apply to these taxa. Location Europe. Methods In order to determine the species tolerances to either low or high temperatures we measured the lethal thermal limits of adults, previously acclimated at one of two temperatures, by means of thermal ramping experiments (± 1°C min^?1). These measures of upper and lower thermal tolerances (UTT and LTT respectively) were then used to estimate each species’ thermal tolerance range, as total thermal tolerance polygons and marginal UTT and LTT thermal polygons. Results Overall, widespread species have higher UTTs and lower LTTs than restricted ones. Mean upper lethal limits of the Agabus brunneus group (43 to 46°C), are similar to those of insects living at similar latitudes, whilst mean lower lethal limits (?6 to ?9°C) are relatively high, suggesting that this group is not particularly cold‐hardy compared with other mid‐temperate‐latitude insects. Widespread species possess the largest thermal tolerance ranges and have a relatively symmetrical tolerance to both high and low temperatures, when compared with range‐restricted relatives. Over the temperature range employed, adults did not acclimate to either high or low temperatures, contrasting with many insect groups, and suggesting that physiological plasticity has a limited role in shaping distribution. Main conclusions Absolute thermal niche appears to be a good predictor of latitudinal range, supporting both Brown’s hypothesis and the environmental variability hypothesis. Restricted‐range species may be more susceptible to the direct effect of climate change than widespread species, notwithstanding the possibility that even ‘thermally‐hardy’, widespread species may be influenced by the indirect effects of climate change such as reduction in habitat availability in Mediterranean areas.     

Thermal sensitivity of a Neotropical amphibian (Engystomops pustulosus) and its vulnerability to climate change

A species’ thermal sensitivity and its exposure to climate variation are key components in the prediction of its vulnerability to climate change. We tested the thermal sensitivity of a tropical amphibian that lives in a mild constant climate in which the thermal tolerance range is expected to closely match the experienced environmental temperature. The air temperature that this species is exposed to varies between 21.9 and 31.6°C with an annual mean of 27.2°C. We estimated the microhabitat water temperature variation under vegetation shade, which buffers the temperature by 1.8°C in relation to that of the air, and with open canopy, where the water was 1.9°C warmer than the air temperature. With broods of tadpoles split into five treatments (15°C, 21°C, 28°C, 31°C, and 33°C), we estimated the critical thermal maximum (CTMax) and critical thermal minimum (CTMin) after at least 7 days of acclimation. Both CTMax (42.3°C) and CTMin (11.8°C) were more extreme than the temperature range estimated for the field. We estimated the optimum temperature (T_o = 28.8°C) and the thermal performance breadth (range: 23.3–34.1°C) based on growth rate (g/day). The animals were able to acclimate more extensively to cold than to warm temperatures. These performance curve traits closely matched the air temperature. The estimated vulnerability varied according to the microhabitat prediction model used. The combination of tadpole data on thermal sensitivity and macro‐ and microhabitat variation provides a necessary framework to understand the effects of climate change on tropical amphibians.     

The evolutionary potential of an insect invader under climate change*

Although the impacts of climate change and invasive species are typically studied in isolation, they likely interact to reduce the viability of plant and animal populations. Indeed, invasive species, by definition, have succeeded in areas outside of their native range and may therefore have higher adaptive capacity relative to native species. Nevertheless, the genetic architecture of the thermal niche, which sets a limit to the potential for populations to evolve rapidly under climate change, has never been measured in an invasive species in its introduced range. Here, we estimate the genetic architecture of thermal performance in the harlequin beetle (Harmonia axyridis), a Central Asian species that has invaded four continents. We measured thermal performance curves in more than 400 third-generation offspring from a paternal half-sib breeding experiment and analyzed the genetic variance–covariance matrix. We show that while the critical thermal limits in this species have an additive genetic basis, most components of the thermal performance curve have low heritability. Moreover, we found evidence that genetic correlations may constrain the evolution of beetles under climate change. Our results suggest that some invasive species may have limited evolutionary capacity under climate change, despite their initial success in colonizing novel environments.     

A Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future

The ability to respond evolutionarily to increasing temperatures is important for survival of ectotherms in a changing climate. Recent studies suggest that upper thermal limits may be evolutionary constrained. We address this hypothesis in a laboratory evolution experiment, encompassing ecologically relevant thermal regimes. To examine the potential for species to respond to climate change, we exposed replicate populations of Drosophila melanogaster to increasing temperatures (0.3 °C every generation) for 20 generations, whereas corresponding replicate control populations were held at benign thermal conditions throughout the experiment. We hypothesized that replicate populations exposed to increasing temperatures would show increased resistance to warm and dry environments compared with replicate control populations. Contrasting replicate populations held at the two thermal regimes showed (i) an increase in desiccation resistance and a decline in heat knock‐down resistance in replicate populations exposed to increasing temperatures, (ii) similar egg‐to‐adult viability and fecundity in replicate populations from the two thermal regimes, when assessed at high stressful temperatures and (iii) no difference in nucleotide diversity between thermal regimes. The limited scope for adaptive evolutionary responses shown in this study highlights the challenges faced by ectotherms under climate change.     

Evolution of thermal performance curves: A meta-analysis of selection experiments

Temperatures are increasing due to global changes, putting biodiversity at risk. Organisms are faced with a limited set of options to cope with this situation: adapt, disperse or die. We here focus on the first possibility, more specifically, on evolutionary adaptations to temperature. Ectotherms are usually characterized by a hump-shaped relationship between fitness and temperature, a non-linear reaction norm that is referred to as thermal performance curve (TPC). To understand and predict impacts of global change, we need to know whether and how such TPCs evolve. Therefore, we performed a systematic literature search and a statistical meta-analysis focusing on experimental evolution and artificial selection studies. This focus allows us to directly quantify relative fitness responses to temperature selection by calculating fitness differences between TPCs from ancestral and derived populations after thermal selection. Out of 7561 publications screened, we found 47 studies corresponding to our search criteria representing taxa across the tree of life, from bacteria, to plants and vertebrates. We show that, independently of species identity, the studies we found report a positive response to temperature selection. Considering entire TPC shapes, adaptation to higher temperatures traded off with fitness at lower temperatures, leading to niche shifts. Effects were generally stronger in unicellular organisms. By contrast, we do not find statistical support for the often discussed “Hotter is better” hypothesis. While our meta-analysis provides evidence for adaptive potential of TPCs across organisms, it also highlights that more experimental work is needed, especially for under-represented taxa, such as plants and non-model systems.