skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, May 23 until 2:00 AM ET on Friday, May 24 due to maintenance. We apologize for the inconvenience.

Title: Feeling the heat: variation in thermal sensitivity within and among populations
ABSTRACT Physiology defines individual responses to global climate change and species distributions across environments. Physiological responses are driven by temperature on three time scales: acute, acclimatory and evolutionary. Acutely, passive temperature effects often dictate an expected 2-fold increase in metabolic processes for every 10°C change in temperature (Q10). Yet, these acute responses often are mitigated through acclimation within an individual or evolutionary adaptation within populations over time. Natural selection can influence both responses and often reduces interindividual variation towards an optimum. However, this interindividual physiological variation is not well characterized. Here, we quantified responses to a 16°C temperature difference in six physiological traits across nine thermally distinct Fundulus heteroclitus populations. These traits included whole-animal metabolism (WAM), critical thermal maximum (CTmax) and substrate-specific cardiac metabolism measured in approximately 350 individuals. These traits exhibited high variation among both individuals and populations. Thermal sensitivity (Q10) was determined, specifically as the acclimated Q10, in which individuals were both acclimated and assayed at each temperature. The interindividual variation in Q10 was unexpectedly large: ranging from 0.6 to 5.4 for WAM. Thus, with a 16°C difference, metabolic rates were unchanged in some individuals, while in others they were 15-fold higher. Furthermore, a significant portion of variation was related to habitat temperature. Warmer populations had a significantly lower Q10 for WAM and CTmax after acclimation. These data suggest that individual variation in thermal sensitivity reflects different physiological strategies to respond to temperature variation, providing many different adaptive responses to changing environments.  more » « less
Award ID(s):
1754437 1556396
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Journal of Experimental Biology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. To better understand temperature's role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus (small estuarine fish) populations from different thermal environments. Fundulus heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographical cline. In this study, we use three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ, and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12 or 28°C, we quantified whole-animal metabolic (WAM) rate, critical thermal maximum (CT max ) and substrate-specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous (i.e. no added substrates)) in approximately 160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within populations. In general, for WAM and CT max , the interindividual variation in acclimation response (log 2 ratio 28/12°C) was a function of performance at 12°C and order of acclimation (12–28°C versus 28–12°C). CT max and WAM were greater at 28°C than 12°C, although WAM had a small change (2.32-fold) compared with the expectation for a 16°C increase in temperature (expect 3- to 4.4-fold). By contrast, for CaM, the rates when acclimatized and assayed at 12 or 28°C were nearly identical. The small differences in CaM between 12 and 28°C temperature were partially explained by cardiac remodeling where individuals acclimatized to 12°C had larger hearts than individuals acclimatized to 28°C. Correlation among physiological traits was dependent on acclimation temperature. For example, WAM was negatively correlated with CT max at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher CaM than fatty acid, and fatty acid supported higher CaM than lactate, ketones and alcohol (LKA) or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These findings suggest interindividual variation in physiological responses to temperature acclimation and indicate that additional research investigating interindividual may be relevant for global climate change responses in many species. 
    more » « less
  2. Abstract

    Adaptive plasticity in thermal tolerance traits may buffer organisms against changing temperatures, making such responses of particular interest in the face of global climate change. Although population variation is integral to the evolvability of this trait, many studies inferring proxies of physiological vulnerability from thermal tolerance traits extrapolate data from one or a few populations to represent the species. Estimates of physiological vulnerability can be further complicated by methodological effects associated with experimental design. We evaluated how populations varied in their acclimation capacity (i.e., the magnitude of plasticity) for critical thermal maximum (CTmax) in two species of tailed frogs (Ascaphidae), cold‐stream specialists. We used the estimates of acclimation capacity to infer physiological vulnerability to future warming. We performed CTmax experiments on tadpoles from 14 populations using a fully factorial experimental design of two holding temperatures (8 and 15°C) and two experimental starting temperatures (8 and 15°C). This design allowed us to investigate the acute effects of transferring organisms from one holding temperature to a different experimental starting temperature, as well as fully acclimated responses by using the same holding and starting temperature. We found that most populations exhibited beneficial acclimation, where CTmax was higher in tadpoles held at a warmer temperature, but populations varied markedly in the magnitude of the response and the inferred physiological vulnerability to future warming. We also found that the response of transferring organisms to different starting temperatures varied substantially among populations, although accounting for acute effects did not greatly alter estimates of physiological vulnerability at the species level or for most populations. These results underscore the importance of sampling widely among populations when inferring physiological vulnerability, as population variation in acclimation capacity and thermal sensitivity may be critical when assessing vulnerability to future warming.

    more » « less
  3. Abstract Physiological trait variation underlies health, responses to global climate change, and ecological performance. Yet, most physiological traits are complex, and we have little understanding of the genes and genomic architectures that define their variation. To provide insight into the genetic architecture of physiological processes, we related physiological traits to heart and brain mRNA expression using a weighted gene co-expression network analysis. mRNA expression was used to explain variation in six physiological traits (whole animal metabolism (WAM), critical thermal maximum (CT max ), and four substrate specific cardiac metabolic rates (CaM)) under 12 °C and 28 °C acclimation conditions. Notably, the physiological trait variations among the three geographically close (within 15 km) and genetically similar F. heteroclitus populations are similar to those found among 77 aquatic species spanning 15–20° of latitude (~ 2,000 km). These large physiological trait variations among genetically similar individuals provide a powerful approach to determine the relationship between mRNA expression and heritable fitness related traits unconfounded by interspecific differences. Expression patterns explained up to 82% of metabolic trait variation and were enriched for multiple signaling pathways known to impact metabolic and thermal tolerance ( e.g. , AMPK, PPAR, mTOR, FoxO, and MAPK) but also contained several unexpected pathways ( e.g. , apoptosis, cellular senescence), suggesting that physiological trait variation is affected by many diverse genes. 
    more » « less
  4. Abstract

    Characterizing thermal acclimation is a common goal of eco‐physiological studies and has important implications for models of climate change and environmental adaptation. However, quantifying thermal acclimation in biological rate processes is not straightforward because many rates increase with temperature due to the acute effect of thermodynamics on molecular interactions. Disentangling such passive plastic responses from active acclimation responses is critical for describing patterns of thermal acclimation.

    Here, we reviewed published studies and distinguished between different study designs measuring the acute (i.e. passive) and acclimated (i.e. active) effects of temperature on metabolic rate. We then developed a method to quantify and classify acclimation responses by comparing acute and acclimatedQ10values. Finally, we applied this method using meta‐analysis to characterize thermal acclimation in metabolic rates of ectothermic animals.

    We reviewed 258 studies measuring thermal effects on metabolic rates, and found that a majority of these studies (74%) did not allow for quantifying the independent effects of acclimation. Such studies were more common when testing aquatic taxa and continue to be published even in recent years.

    A meta‐analysis of 96 studies where acclimation could be quantified (using 1,072Q10values) revealed that ‘partial compensation’ was the most common acclimation response (i.e. acclimation tended to offset the passive change in metabolic rate due to acute temperature changes). However, ‘no acclimation’ and ‘inverse compensation’, in which acclimation further augmented the acute change in metabolic rate, were also common.

    Acclimation responses differed among taxa, habitats and with experimental design. Amphibians and other terrestrial taxa tended to show weak acclimation responses, whereas fishes and other aquatic taxa tended to show stronger compensatory responses. Increasing how long the animal was allowed to adjust to a new test temperature increased the acclimation response, but body size did not. Acclimation responses were also stronger with longer acclimation durations.

    Collectively, these results highlight the importance of using the appropriate experimental design to investigate and estimate thermal acclimation of biological rates. To facilitate and guide future studies of thermal acclimation, we end with some suggestions for designing and interpreting experiments.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

    more » « less
  5. Abstract

    Predicting the potential effects of changes in climate on freshwater species requires an understanding of the relationships between physiological traits and environmental conditions among populations. While water temperature is a primary factor regulating metabolic rates in freshwater ectotherms, how metabolic rates vary across the species range is unclear. In addition, photoperiod has also been hypothesised to influence metabolic rates in freshwater taxa based on seasonal changes in activity rates. Using an experimental approach, we investigated whether variation in routine metabolic rate (RMR) and sensitivity of RMR to changes in temperature are correlated with local thermal regimes, photoperiods and body mass among ten populations across the geographic range of the Bluntnose minnow (Pimephales notatus), a North American freshwater fish species. Routine metabolic rate data were collected from populations acclimatised to three temperature treatments (9, 18 and 27°C) and correlated with water temperature and photoperiod estimates at collection locations for each population. Routine metabolic rate was negatively correlated with minimum photoperiod at 9°C, negatively correlated with weekly high temperature at 18°C and positively correlated with weekly high temperature at 27°C. Body mass was also a predictor of RMR at each temperature treatment. Thermal sensitivity of RMR was positively correlated with weekly high temperature, indicating that individuals from warmer low latitude populations experienced greater sensitivity of RMR to changes in temperature than individuals from cooler high latitude populations. These results indicate differential responses among populations to variation in temperature and suggest the importance of recognising this variation when characterising responses of freshwater taxa to increases in water temperature.

    more » « less