RESUMEN

Amphibians and fishes play a central role in shaping the structure and function of freshwater environments. These organisms have a limited capacity to disperse across different habitats and the thermal buffer offered by freshwater systems is small. Understanding determinants and patterns of their physiological sensitivity across life history is, therefore, imperative to predicting the impacts of climate change in freshwater systems. Based on a systematic literature review including 345 experiments with 998 estimates on 96 amphibian (Anura/Caudata) and 93 freshwater fish species (Teleostei), we conducted a quantitative synthesis to explore phylogenetic, ontogenetic, and biogeographic (thermal adaptation) patterns in upper thermal tolerance (CTmax) and thermal acclimation capacity (acclimation response ratio, ARR) as well as the influence of the methodology used to assess these thermal traits using a conditional inference tree analysis. We found globally consistent patterns in CTmax and ARR, with phylogeny (taxa/order), experimental methodology, climatic origin, and life stage as significant determinants of thermal traits. The analysis demonstrated that CTmax does not primarily depend on the climatic origin but on experimental acclimation temperature and duration, and life stage. Higher acclimation temperatures and longer acclimation times led to higher CTmax values, whereby Anuran larvae revealed a higher CTmax than older life stages. The ARR of freshwater fishes was more than twice that of amphibians. Differences in ARR between life stages were not significant. In addition to phylogenetic differences, we found that ARR also depended on acclimation duration, ramping rate, and adaptation to local temperature variability. However, the amount of data on early life stages is too small, methodologically inconsistent, and phylogenetically unbalanced to identify potential life cycle bottlenecks in thermal traits. We, therefore, propose methods to improve the robustness and comparability of CTmax/ARR data across species and life stages, which is crucial for the conservation of freshwater biodiversity under climate change.

Asunto(s)

RESUMEN

Most ectotherms rely on behavioural thermoregulation to maintain body temperatures close to their physiological optimum. Hence, ectotherms can drastically limit their exposure to thermal extremes by selecting a narrower range of temperatures, which includes their preferred temperature (Tpref). Despite evidence that behavioural thermoregulation can be adjusted by phenotypic plasticity or constrained by natural selection, intraspecific Tpref variations across environmental gradients remain overlooked as compared to other thermal traits like thermal tolerance. Here, we analyzed Tpref variation of spider populations found along a gradient of urban heat island (UHI) which displays large thermal variations over small distances. We measured two components of the thermal preference, namely the mean Tpref and the Tpref range (i.e., standard deviation) in 557 field-collected individuals of a common ground-dwelling spider (Pardosa saltans, Lycosidae) using a laboratory thermal gradient. We determined if Tpref values differed among ten populations from contrasting thermal zones. We showed that endogenous factors such as body size or sex primarily determine both mean Tpref and Tpref range. The Tpref range was also linked to the UHI intensity to a lesser extent, yet only in juveniles. The absence of relationship between Tpref metrics and UHI in adult spiders suggests a Bogert effect according to which the ability of individuals to detect and exploit optimal microclimates weakens the selection pressure of temperatures (here driven by UHI) on their thermal physiology. Alternatively, this lack of relationship could also indicate that temperature patterns occurring at the scale of the spiders' micro-habitat differ from measured ones. This study shows the importance of considering both inter-individual and inter-population variations of the Tpref range when conducting Tpref experiments, and supports Tpref range as being a relevant measure to inform on the strength of behavioural thermoregulation in a given population.

RESUMEN

Species with large geographical ranges provide an excellent model for studying how different populations respond to dissimilar local conditions, particularly with respect to variation in climate. Maternal effects, such as nest-site choice greatly affect offspring phenotypes and survival. Thus, maternal behaviour has the potential to mitigate the effects of divergent climatic conditions across a species' range. We delineated natural nesting areas of six populations of painted turtles (Chrysemys picta) that span a broad latitudinal range and quantified spatial and temporal variation in nest characteristics. To quantify microhabitats available for females to choose, we also identified sites within the nesting area of each location that were representative of available thermal microhabitats. Across the range, females nested non-randomly and targeted microhabitats that generally had less canopy cover and thus higher nest temperatures. Nest microhabitats differed among locations but did not predictably vary with latitude or historic mean air temperature during embryonic development. In conjunction with other studies of these populations, our results suggest that nest-site choice is homogenizing nest environments, which buffers embryos from thermally induced selection and could slow embryonic evolution. Thus, although effective at a macroclimatic scale, nest-site choice is unlikely to compensate for novel stressors that rapidly increase local temperatures. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Asunto(s)

RESUMEN

The vulnerability of species to climate change is jointly influenced by geographic phenotypic variation, acclimation and behavioural thermoregulation. The importance of interactions between these factors, however, remains poorly understood. We demonstrate how advances in mechanistic niche modelling can be used to integrate and assess the influence of these sources of uncertainty in forecasts of climate change impacts. We explored geographic variation in thermal tolerance (i.e. maximum and minimum thermal limits) and its potential for acclimation in juvenile European common frogs Rana temporaria along elevational gradients. Furthermore, we employed a mechanistic niche model (NicheMapR) to assess the relative contributions of phenotypic variation, acclimation and thermoregulation in determining the impacts of climate change on thermal safety margins and activity windows. Our analyses revealed that high-elevation populations had slightly wider tolerance ranges driven by increases in heat tolerance but lower potential for acclimation. Plausibly, wider thermal fluctuations at high elevations favour more tolerant but less plastic phenotypes, thus reducing the risk of encountering stressful temperatures during unpredictable extreme events. Biophysical models of thermal exposure indicated that observed phenotypic and plastic differences provide limited protection from changing climates. Indeed, the risk of reaching body temperatures beyond the species' thermal tolerance range was similar across elevations. In contrast, the ability to seek cooler retreat sites through behavioural adjustments played an essential role in buffering populations from thermal extremes predicted under climate change. Predicted climate change also altered current activity windows, but high-elevation populations were predicted to remain more temporally constrained than lowland populations. Our results demonstrate that elevational variation in thermal tolerances and acclimation capacity might be insufficient to buffer temperate amphibians from predicted climate change; instead, behavioural thermoregulation may be the only effective mechanism to avoid thermal stress under future climates.

Asunto(s)

RESUMEN

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.

Asunto(s)

RESUMEN

The role of behavior in evolution has long been discussed, with some arguing that behavior promotes evolution by exposing organisms to selection (behavioral drive) and others proposing that it inhibits evolution by shielding organisms from environmental variation (behavioral inertia). However, this discussion has generally focused on the effects of behavior along a single axis without considering that behavior simultaneously influences selection in various niche dimensions. By examining evolutionary change along two distinct niche axes-structural and thermal-we propose that behavior simultaneously drives and impedes evolution in a group of Anolis lizards from the Caribbean island of Hispaniola. Specifically, a behavioral shift in microhabitat to boulders at high altitude enables thermoregulation, thus forestalling physiological evolution in spite of colder environments. This same behavioral shift drives skull and limb evolution to boulder use. Our results emphasize the multidimensional effects of behavior in evolution. These findings reveal how, rather than being diametrically opposed, niche conservatism and niche lability can occur simultaneously. Furthermore, patterns of niche evolution may vary at different geographic scales: because of thermoregulatory behavior, lizards at high and low elevation share similar microclimatic niches (consistent with niche conservatism) while inhabiting distinct macroclimatic environments (consistent with niche divergence). Together, our results suggest that behavior can connect patterns of niche divergence and conservatism at different geographic scales and among traits.

Asunto(s)

RESUMEN

Heat tolerance is a trait of paramount ecological importance and may determine a species' ability to cope with ongoing climate change. Although critical thermal limits have consequently received substantial attention in recent years, their potential variation throughout ontogeny remained largely neglected. We investigate whether such neglect may bias conclusions regarding a species' sensitivity to climate change. Using a tropical butterfly, we found that developmental stages clearly differed in heat tolerance. It was highest in pupae followed by larvae, adults and finally eggs and hatchlings. Strikingly, most of the variation found in thermal tolerance was explained by differences in body mass, which may thus impose a severe constraint on adaptive variation in stress tolerance. Furthermore, temperature acclimation was beneficial by increasing heat knock-down time and therefore immediate survival under heat stress, but it affected reproduction negatively. Extreme temperatures strongly reduced survival and subsequent reproductive success even in our highly plastic model organism, exemplifying the potentially dramatic impact of extreme weather events on biodiversity. We argue that predictions regarding a species' fate under changing environmental conditions should consider variation in thermal tolerance throughout ontogeny, variation in body mass and acclimation responses as important predictors of stress tolerance.

Asunto(s)

RESUMEN

Thermal tolerance varies at all hierarchical levels of biological organization: among species, populations, individuals, and even within individuals. Age- or developmental stage- and sex-specific thermal effects have received relatively little attention in the literature, despite being crucial for understanding thermal adaptation in nature and responses to global warming. We document stage- and sex- specific heat tolerance in the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae), a species common throughout the northern hemisphere that generally favours cool climates. Exposure of eggs to temperatures up to 32°C did not affect larval hatching rate, but subsequent egg-to-adult survival at a benign temperature was reduced. Permanent transfer from benign (18°C) to hot temperatures (up to 31°C) at different larval and pupal stages strongly decreased egg-to-adult survival, though survival continuously improved the later the transfer occurred. Temporary transfer for only two days increased mortality more weakly, survival being lowest when temperature stress was imposed early during the larval or pupal stages. Adult flies provided with sugar and water tolerated 31°C longer than previously thought (5 days in males to 9 days in females). Eggs were thus less susceptible to thermal stress than larvae, pupae or adults, in agreement with the hypothesis that more mobile stages require less physiological protection against heat because they can behaviourally thermoregulate. The probability of mating, of laying a clutch, and hatching success were generally independently reduced by exposure of females or males to warm temperatures (24°C) during the juvenile or adult stages, with some interactions evident. High temperature stress thus affects survival differentially depending on when it occurs during the juvenile or the pre-reproductive adult life stage, and affects reproductive success via the mating behaviour of both sexes, female physiology in terms of oviposition, and fertility via sperm and/or egg quality. Our results illustrate that temperature stress, even when moderate and temporary, during early development can have profound lethal and non-lethal fitness-consequences later in life.

Asunto(s)

RESUMEN

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.

Asunto(s)