Temperature Variability and Metabolic Adaptation in Terrestrial and Aquatic Ectotherms

Thermodynamics is a major factor determining rates of biochemical processes, rates of energy expenditure and ultimately resilience to global warming in ectothermic organisms. Nonetheless, whether ectothermic organisms exhibit general adaptive metabolic responses to cope with different thermal conditions remains a highly contentious subject for decades. Here we combine a model comparison approach with a global dataset of standard metabolic rates (SMR), which include 1,160 measurements across 788 species of aquatic invertebrates, insects, fishes, amphibians and reptiles, to investigate the association between metabolic levels and geographic variation in environmental temperatures. According to Akaike’s information criterion (AICc), the variation in SMR after removing allometric and thermodynamic effects is best explained by the range of temperatures encountered along the annual cycle, which provided consistently a better fit than the average temperature for the hottest and coldest month as well as mean annual temperatures. This pattern was consistent across taxonomic groups and robust to sensitivity analyses. Nonetheless, aquatic and terrestrial lineages responded differently to seasonality, with SMR declining –6.8 % ºC–1 of temperature variation in aquatic organisms and increasing 2.8 % ºC– 1 in terrestrial. These responses reflect alternative strategies to mitigate the impact of warmer temperatures on energy expenditure, either by means of metabolic reduction in thermally stable water bodies or effective behavioral thermoregulation to exploit temperature heterogeneity on land.

Greater local adaptation to temperature in the ocean than on land

Warming threatens biodiversity but there is considerable uncertainty in which species and ecosystems are most vulnerable. Moreover, our understanding of organismal sensitivity is largely centered on species level assessments, which do not consider variation across populations. Here, we used meta-analysis to quantify differentiation in thermal tolerance across 413 populations from 105 species living in terrestrial, marine, and freshwater realms. Strikingly, we found strong differentiation in heat tolerance across populations in marine and intertidal taxa but not terrestrial or freshwater taxa. This is counter to the expectation that increased dispersal potential in the ocean should reduce intraspecific variation. Our findings are consistent with the “Bogert effect” operating in terrestrial but not marine ecosystems, which predicts that behavioral thermoregulation constrains evolution. Such adaptive differentiation in the ocean suggests that there may be standing genetic variation at the species level to buffer climate impacts. Assessments of organismal vulnerability to warming, especially in marine species, should account for variation in thermal tolerance among populations or risk under- or overestimating climate vulnerability.

Evolution of Thermal Sensitivity in Changing and Variable Climates

Evolutionary adaptation to temperature and climate depends on both the extent to which organisms experience spatial and temporal environmental variation (exposure) and how responsive they are to the environmental variation (sensitivity). Theoretical models and experiments suggesting substantial potential for thermal adaptation have largely omitted realistic environmental variation. Environmental variation can drive fluctuations in selection that slow adaptive evolution. We review how carefully filtering environmental conditions based on how organisms experience their environment and further considering organismal sensitivity can improve predictions of thermal adaptation. We contrast taxa differing in exposure and sensitivity. Plasticity can increase the rate of evolutionary adaptation in taxa exposed to pronounced environmental variation. However, forms of plasticity that severely limit exposure, such as behavioral thermoregulation and phenological shifts, can hinder thermal adaptation. Despite examples of rapid thermal adaptation, experimental studies often reveal evolutionary constraints. Further investigating these constraints and issues of timescale and thermal history are needed to predict evolutionary adaptation and, consequently, population persistence in changing and variable environments. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Effects Of Acclimation, Population, And Sex On Behavioral Thermoregulation, CTMax, Symptoms Of Heat Stress, And Gene Expression of Melanoplus Differentialis, A Generalist Grasshopper - Does Temporal Thermal Heterogeneity Prepare Populations For A Warming World?

Insects thermoregulate using both canalized and plastic mechanisms. Populations of insects utilize these mechanisms to different extents, and while it is posited that the degree of thermal fluctuation a population experiences can determine the optimal combination of mechanisms to utilize, this is still being elucidated. We used three populations of the generalist grasshopper, Melanoplus differentialis (Thomas, 1856), from sites experiencing different degrees of thermal heterogeneity to test for correlations between thermal heterogeneity and 1) behavioral thermoregulation, 2) upper temperature tolerance, 3) the ability to thermally acclimate, and 4) gene expression. We found that 1) behavioral thermoregulation did not differ among sites, 2) CTMax of males, but not females, was higher at more thermally heterogeneous sites, 3) there was acclimation in some of the tested traits, but thermally heterogeneous sites did not always have the most plastic individuals, and 4) there were differences in gene expression among sites, but these differences were not between the most and least thermally heterogeneous sites. We concluded that thermal heterogeneity may play a selective role in some, but not all, of the measured thermoregulatory traits and their plasticity.

Thermal Sensitivity of Heat Sensor TRPA1 Correlates With Temperatures Inducing Heat Avoidance Behavior in Terrestrial Ectotherms

Temperature is an essential environmental factor that controls an organism’s performances. As ectothermic animals largely rely on external heat sources for adjusting their body temperature, thermal perception is a primary process of behavioral thermoregulation. Transient receptor potential ankyrin 1 (TRPA1) is a heat sensitive ion channel in most non-mammalian species, and its heat activation has been suggested to induce heat avoidance behaviors in ectothermic animals. However, associations between TRPA1 and ecologically relevant temperatures have not been investigated, and the analyses including diverse taxa will provide robust support for understanding the associations. Here, I conducted extensive literature review, and assembled published data on thermal threshold of TRPA1 and three physiological parameters: the experimental voluntary maximum (EVM), which is body temperatures when heat avoidance behaviors are induced; the critical thermal maximum (CTmax), which is a point in temperature beyond which an organism becomes incapacitated; and average body temperature (Tmean) recorded in the field. Then, I examined the relationships between thermal threshold of TRPA1 and each of the three physiological parameters. As phylogenetically closely related species tend to show similar trait values among species, I conducted the regression analyses by accounting for phylogenetic distances among species. This study supports previous research by affirming that thermal threshold of TRPA1 is substantially correlated with body temperature that the animals escaped from the heat source, represented here as EVM. Nevertheless, thermal threshold of TRPA1 showed a statistically insignificant correlation with CTmax and Tmean. The results suggest that although thermal threshold of TRPA1 is evolutionarily labile, its associations with EVM is highly conserved among diverse terrestrial ectotherms. Therefore, thermal threshold of TRPA1 could be a useful parameter to evaluate species vulnerability to thermal stress particularly in the recent climate warming scenario.

Vulnerability to climate change of a microendemic lizard species from the central Andes

Given the rapid loss of biodiversity as consequence of climate change, greater knowledge of ecophysiological and natural history traits are crucial to determine which environmental factors induce stress and drive the decline of threatened species. Liolaemus montanezi (Liolaemidae), a xeric-adapted lizard occurring only in a small geographic range in west-central Argentina, constitutes an excellent model for studies on the threats of climate change on such microendemic species. We describe field data on activity patterns, use of microhabitat, behavioral thermoregulation, and physiology to produce species distribution models (SDMs) based on climate and ecophysiological data. Liolaemus montanezi inhabits a thermally harsh environment which remarkably impacts their activity and thermoregulation. The species shows a daily bimodal pattern of activity and mostly occupies shaded microenvironments. Although the individuals thermoregulate at body temperatures below their thermal preference they avoid high-temperature microenvironments probably to avoid overheating. The population currently persists because of the important role of the habitat physiognomy and not because of niche tracking, seemingly prevented by major rivers that form boundaries of their geographic range. We found evidence of habitat opportunities in the current range and adjacent areas that will likely remain suitable to the year 2070, reinforcing the relevance of the river floodplain for the species’ avoidance of extinction.

Dehydration Alters Behavioral Thermoregulation and the Geography of Climatic Vulnerability in Amazonian Lizards

Since high temperatures and low water availability often strike organisms in parallel, observing how they behaviorally thermohydroregulate may help us to better understand their climatic vulnerability. This understanding is especially important for tropical lizards, purportedly under greater climatic risk. We observed the influence of hydration level on the Voluntary Thermal Maximum (VTM) of two small amazonian lizard species: Loxopholis ferreirai (semiaquatic and scansorial) and Loxopholis percarinatum (leaf litter parthenogenetic dweller), accounting for several sources of variation (turn, body weight, start temperature and heating rate). Then, we used two modelling approaches (simple mapping of thermal margins and NicheMapR), to examine the effects of dehydration, decrease in rainfall, ability to burrow, and tree cover availability, on the geography of climatic vulnerability. Dehydration decreased the VTM in both species, which also reacted to start temperature and heating rates. Our two modelling approaches show that dehydration, changes the intensity, extent and duration of thermal risk across the Amazon basin. Based on our results and previous studies, we identify new evidence needed to better understand thermohydroregulation and model the geography of climatic risk, more realistically.