Variation In Thermal Plasticity Research Articles

Among-individual variation in thermal plasticity of fish metabolic rates causes profound variation in temperature-specific trait repeatability, but does not co-vary with behavioural plasticity.

Conspecifics of the same age and size differ consistently in the pace with which they expend energy. This among-individual variation in metabolic rate is thought to influence behavioural variation, since differences in energy requirements should motivate behaviours that facilitate energy acquisition, such as being bold or active in foraging. While there is evidence for links between metabolic rate and behaviour in constant environments, we know little about whether metabolic rate and behaviour change together when the environment changes-that is, if metabolic and behavioural plasticity co-vary. We investigated this using a fish that becomes dormant in winter and strongly reduces its activity when the environment cools, the cunner (Tautogolabrus adspersus). We found strong and predictable among-individual variation in thermal plasticity of metabolic rates, from resting to maximum levels, but no evidence for among-individual variation in thermal plasticity of movement activity, meaning that these key physiological and behavioural traits change independently when the environment changes. The strong among-individual variation in metabolic rate plasticity resulted in much higher repeatability (among-individual consistency) of metabolic rates at warm than cold temperatures, indicating that the potential for metabolic rate to evolve under selection is temperature-dependent, as repeatability can set the upper limit to heritability. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Impact of developmental temperatures on thermal plasticity and repeatability of metabolic rate

Phenotypic plasticity is an important mechanism that allows populations to adjust to changing environments. Early life experiences can have lasting impacts on how individuals respond to environmental variation later in life (i.e., individual reaction norms), altering the capacity for populations to respond to selection. Here, we incubated lizard embryos (Lampropholis delicata) at two fluctuating developmental temperatures (cold = 23 ºC + / − 3 ºC, hot = 29 ºC + / − 3 ºC, ncold = 26, nhot = 25) to understand how it affected metabolic plasticity to temperature later in life. We repeatedly measured individual reaction norms across six temperatures 10 times over ~ 3.5 months (nobs = 3,818) to estimate the repeatability of average metabolic rate (intercept) and thermal plasticity (slope). The intercept and the slope of the population-level reaction norm was not affected by developmental temperature. Repeatability of average metabolic rate was, on average, 10% lower in hot incubated lizards but stable across all temperatures. The slope of the thermal reaction norm was overall moderately repeatable (R = 0.44, 95% CI = 0.035 – 0.93) suggesting that individual metabolic rate changed consistently with short-term changes in temperature, although credible intervals were quite broad. Importantly, reaction norm repeatability did not depend on early developmental temperature. Identifying factors affecting among-individual variation in thermal plasticity will be increasingly more important for terrestrial ectotherms living in changing climate. Our work implies that thermal metabolic plasticity is robust to early developmental temperatures and has the capacity to evolve, despite there being less consistent variation in metabolic rate under hot environments.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Individual variation in thermal plasticity and its impact on mass‐scaling

Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass‐scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass‐scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months (N[observations] = 4952). Using hierarchical statistical techniques, we accounted for multi‐level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass‐scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (Rslope = 0.25, 95% CI = 2.48 × 10−8 – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross‐temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass‐scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.

Temporal variation in thermal plasticity in a free-ranging subalpine lizard.

Thermally variable environments are particularly challenging for ectotherms as physiological functions are thermo-dependent. As a consequence, ectotherms in highly seasonal environments are predicted to have greater thermal plasticity. However, much of our understanding of thermal plasticity comes from controlled experiments in a laboratory setting. Relatively fewer studies investigate thermal plasticity in free-ranging animals living in their natural environment. We investigated the presence of thermal plasticity within a single activity season in adult males of a natural high elevation population of White's skink (Liopholis whitii) in south-eastern Australia. This species lives in a permanent home site (rock crevice and/or burrow), facilitating the repeated capture of the same individuals across the activity season. We monitored the thermal variation across the field site and over the activity season, and tested thermal tolerances and performance of male L. whitii on three occasions across their activity season. Maximum and average temperatures varied across the field site, and temperatures gradually increased across the study period. Evidence of temporal plasticity was identified in the critical thermal minimum and thermal tolerance breadth, but not in the critical thermal maximum. Thermal performance was also found to be plastic, but no temporal patterns were evident. Our temporal plasticity results are consistent which much of the previous literature, but this is one of the first studies to identify these patterns in a free-ranging population. In addition, our results indicate that performance may be more plastic than previous literature suggests. Overall, our study highlights the need to pair laboratory and field studies in order to understand thermal plasticity in an ecologically relevant context.

Will like replace like? Linking thermal performance to ecological function across predator and herbivore populations.

The inability of species to adapt to changing climate may cause ecological communities to disassemble and lose ecological functioning. However, theory suggests that communities may be resilient whenever populations within species exhibit variation in thermal plasticity or adaptation whereby thermally tolerant populations replace thermally sensitive ones. But will they maintain the functional roles of the populations being replaced? This study evaluated whether "like replaces like" functionally by measuring how four populations of a grasshopper herbivore and its co-occurring spider predator cope with environmental warming. The study occurred across a latitudinal gradient bounded by southerly, warmer Connecticut and northerly, cooler New Hampshire, USA. The study compared the survival rates, thermal performance, habitat usage, and food chain interactions of each grasshopper and spider population between its home field site (field of origin) and a Connecticut transplant site, and the native Connecticut population. Three grasshopper populations exhibited physiological plasticity by adjusting metabolic rates. The fourth population selected cooler habitat locations. Spider populations did not alter their metabolism and instead selected cooler habitat locations, thereby altering spatial overlap with their prey and food chain interactions. Grasshopper populations that coped physiologically consumed plants in different ratios than the fourth population and the Connecticut population. Hence, "like may not replace like" whenever populations adapt physiologically to warming.

Ontogenetic changes in genetic variances of age-dependent plasticity along a latitudinal gradient.

The expression of phenotypic plasticity may differ among life stages of the same organism. Age-dependent plasticity can be important for adaptation to heterogeneous environments, but this has only recently been recognized. Whether age-dependent plasticity is a common outcome of local adaptation and whether populations harbor genetic variation in this respect remains largely unknown. To answer these questions, we estimated levels of additive genetic variation in age-dependent plasticity in six species of damselflies sampled from 18 populations along a latitudinal gradient spanning 3600 km. We reared full sib larvae at three temperatures and estimated genetic variances in the height and slope of thermal reaction norms of body size at three points in time during ontogeny using random regression. Our data show that most populations harbor genetic variation in growth rate (reaction norm height) in all ontogenetic stages, but only some populations and ontogenetic stages were found to harbor genetic variation in thermal plasticity (reaction norm slope). Genetic variances in reaction norm height differed among species, while genetic variances in reaction norm slope differed among populations. The slope of the ontogenetic trend in genetic variances of both reaction norm height and slope increased with latitude. We propose that differences in genetic variances reflect temporal and spatial variation in the strength and direction of natural selection on growth trajectories and age-dependent plasticity. Selection on age-dependent plasticity may depend on the interaction between temperature seasonality and time constraints associated with variation in life history traits such as generation length.

Variation in spawning time promotes genetic variability in population responses to environmental change in a marine fish.

The level of phenotypic plasticity displayed within a population (i.e. the slope of the reaction norm) reflects the short-term response of a population to environmental change, while variation in reaction norm slopes among populations reflects spatial variation in these responses. Thus far, studies of thermal reaction norm variation have focused on geographically driven adaptation among different latitudes, altitudes or habitats. Yet, thermal variability is a function of both space and time. For organisms that reproduce at different times of year, such variation has the potential to promote adaptive variability in thermal responses for critical early life stages. Using common-garden experiments, we examined the spatial scale of genetic variation in thermal plasticity for early life-history traits among five populations of endangered Atlantic cod (Gadus morhua) that spawn at different times of year. Patterns of plasticity for larval growth and survival suggest that population responses to climate change will differ substantially, with increasing water temperatures posing a considerably greater threat to autumn-spawning cod than to those that spawn in winter or spring. Adaptation to seasonal cooling or warming experienced during the larval stage is suggested as a possible cause. Furthermore, populations that experience relatively cold temperatures during early life might be more sensitive to changes in temperature. Substantial divergence in adaptive traits was evident at a smaller spatial scale than has previously been shown for a marine fish with no apparent physical barriers to gene flow (∼200 km). Our findings highlight the need to consider the impact of intraspecific variation in reproductive timing on thermal adaptation when forecasting the effects of climate change on animal populations.

Developmental thermal plasticity among Drosophila melanogaster populations.

Many biotic and abiotic variables influence the dispersal and distribution of organisms. Temperature has a major role in determining these patterns because it changes daily, seasonally and spatially, and these fluctuations have a significant impact on an organism's behaviour and fitness. Most ecologically relevant phenotypes that are adaptive are also complex and thus they are influenced by many underlying loci that interact with the environment. In this study, we quantified the degree of thermal phenotypic plasticity within and among populations by measuring chill-coma recovery times of lines reared from egg to adult at two different environmental temperatures. We used sixty genotypes from six natural populations of Drosophila melanogaster sampled along a latitudinal gradient in South America. We found significant variation in thermal plasticity both within and among populations. All populations exhibit a cold acclimation response, with flies reared at lower temperatures having increased resistance to cold. We tested a series of environmental parameters against the variation in population mean thermal plasticity and discovered the mean thermal plasticity was significantly correlated with altitude of origin of the population. Pairing our data with previous experiments on viability fitness assays in the same populations in fixed and variable environments suggests an adaptive role of this thermal plasticity in variable laboratory environments. Altogether, these data demonstrate abundant variation in adaptive thermal plasticity within and among populations.

Capacity for thermal acclimation differs between populations and phylogenetic lineages within a species

Summary Within‐individual plasticity (acclimation) counteracts potentially negative physiological effects resulting from environmental changes and thereby maintains fitness across a broad range of environments. The capacity for the acclimation of individuals may therefore determine the persistence of populations in variable environments. We determined phylogenetic relationships by Amplified Fragment Length Polymorphism (AFLP) analysis of six populations of mosquitofish (Gambusia holbrooki) from coastal and mountain environments and compared their capacity for thermal acclimation to test the hypotheses that acclimation capacity is greater in more seasonal environments with less diurnal variability, that acclimation is genetically constrained and that demographic processes determine acclimation capacity. We show that populations are divided into distinct genetic lineages and that populations within lineages have distinct genetic identities. There were significant differences in the capacity for acclimation between traits (swimming performance, citrate synthase and lactate dehydrogenase activities), between lineages and between populations within lineages. We rejected the hypothesis that climatic conditions (coastal vs. mountain) determined the capacity for acclimation, but accepted the hypotheses that demographic processes and genetic constraint influenced thermal acclimation. The importance of our data lies in proof of concept that there can be substantial variation in thermal plasticity between populations within species. Similar responses are likely to be found in other species that comprise structured populations. Many predictions of the impact of climate change on biodiversity assume a species‐specific response to changing environments. Based on our results, we argue that this resolution can be too coarse and that analysis of the impacts of climate change and other environmental variability should be resolved to a population level.

Geographic variation in thermal plasticity of life history and wing pattern in Bicyclus anynana

Temperature is one of the main environmental cues regulating seasonal plasticity in insects. Global climate change may lead to a change in the predictive value of temperature for sea- sonal conditions, potentially resulting in a mismatch of phenotypic form and environment. The afrotropical butterfly Bicyclus anynana shows striking seasonal plasticity for wing patterns and life history traits. This polyphenism is an adaptation to contrasting patterns of rainfall over wet and dry seasons, and is mainly determined by temperature. To investigate the extent of local adaptation of the developmental plasticity response to regional climate, we compared the thermal reaction norms for several life history traits and wing pattern of 2 distant populations from regions with different tem- perature-rainfall associations. We found little to no population differentiation for the life history traits, while wing pattern showed substantially more geographic variation. Broad-sense heritabilities and cross-environment correlations for wing pattern and 2 life history traits indicated a potential for adaptation of the plasticity response of these traits. Our results indicate that thermal plasticity of wing pattern can be population-specific; thus climate change may lead to a mismatch of wing pattern to seasonal environment. Traits that can be further modified by acclimation during the butterfly's adult life span (starvation resistance, resting metabolic rate and egg size) showed no geographic differen- tiation for their developmental plasticity. This indicates that for these traits, adult acclimation plays an important role in coping with local climate.