Variation In Thermal Tolerance Research Articles

Improving growth models of cultivated sugar kelp, Saccharina latissima, by accounting for intraspecific variation in thermal tolerance

Improving growth models of cultivated sugar kelp, <i>Saccharina latissima</i>, by accounting for intraspecific variation in thermal tolerance

Environmental and Biogeographic Drivers behind Alpine Plant Thermal Tolerance and Genetic Variation.

In alpine ecosystems, elevation broadly functions as a steep thermal gradient, with plant communities exposed to regular fluctuations in hot and cold temperatures. These conditions lead to selective filtering, potentially contributing to species-level variation in thermal tolerance and population-level genetic divergence. Few studies have explored the breadth of alpine plant thermal tolerances across a thermal gradient or the underlying genetic variation thereof. We measured photosystem heat (Tcrit-hot) and cold (Tcrit-cold) thresholds of ten Australian alpine species across elevation gradients and characterised their neutral genetic variation. To reveal the biogeographical drivers of present-day genetic signatures, we also reconstructed temporal changes in habitat suitability across potential distributional ranges. We found intraspecific variation in thermal thresholds, but this was not associated with elevation, nor underpinned by genetic differentiation on a local scale. Instead, regional population differentiation and considerable homozygosity within populations may, in part, be driven by distributional contractions, long-term persistence, and migrations following habitat suitability. Our habitat suitability models suggest that cool-climate-distributed alpine plants may be threatened by a warming climate. Yet, the observed wide thermal tolerances did not reflect this vulnerability. Conservation efforts should seek to understand variations in species-level thermal tolerance across alpine microclimates.

Unique photosynthetic strategies employed by closely related Breviolum minutum strains under rapid short-term cumulative heat stress.

The thermal tolerance of symbiodiniacean photo-endosymbionts largely underpins the thermal bleaching resilience of their cnidarian hosts such as corals and the coral model Exaiptasia diaphana. While variation in thermal tolerance between species is well documented, variation between conspecific strains is understudied. We compared the thermal tolerance of three closely related strains of Breviolum minutum represented by two internal transcribed spacer region 2 profiles (one strain B1-B1o-B1g-B1p and the other two strains B1-B1a-B1b-B1g) and differences in photochemical and non-photochemical quenching, de-epoxidation state of photopigments, and accumulation of reactive oxygen species under rapid short-term cumulative temperature stress (26-40 °C). We found that B. minutum strains employ distinct photoprotective strategies, resulting in different upper thermal tolerances. We provide evidence for previously unknown interdependencies between thermal tolerance traits and photoprotective mechanisms that include a delicate balancing of excitation energy and its dissipation through fast relaxing and state transition components of non-photochemical quenching. The more thermally tolerant B. minutum strain (B1-B1o-B1g-B1p) exhibited an enhanced de-epoxidation that is strongly linked to the thylakoid membrane melting point and possibly membrane rigidification minimizing oxidative damage. This study provides an in-depth understanding of photoprotective mechanisms underpinning thermal tolerance in closely related strains of B. minutum.

Complex parental effects impact variation in larval thermal tolerance in a vertically transmitting coral.

Coral populations must be able to adapt to changing environmental conditions for coral reefs to persist under climate change. The adaptive potential of these organisms is difficult to forecast due to complex interactions between the host animal, dinoflagellate symbionts and the environment. Here we created 26 larval families from six Montipora capitata colonies from a single reef, showing significant, heritable variation in thermal tolerance. Our results indicate that 9.1% of larvae are expected to exhibit four times the thermal tolerance of the general population. Differences in larval thermotolerance were driven mainly by maternal contributions, but we found no evidence that these effects were driven by symbiont identity despite vertical transmission from the dam. We also document no evidence of reproductive incompatibility attributable to symbiont identity. These data demonstrate significant genetic variation within this population which provides the raw material upon which natural selection can act.

Phenotypic adaptation to temperature in the mosquito vector, Aedes aegypti.

Most models exploring the effects of climate change on mosquito-borne disease ignore thermal adaptation. However, if local adaptation leads to changes in mosquito thermal responses, "one size fits all" models could fail to capture current variation between populations and future adaptive responses to changes in temperature. Here, we assess phenotypic adaptation to temperature in Aedes aegypti, the primary vector of dengue, Zika, and chikungunya viruses. First, to explore whether there is any difference in existing thermal response of mosquitoes between populations, we used a thermal knockdown assay to examine five populations of Ae. aegypti collected from climatically diverse locations in Mexico, together with a long-standing laboratory strain. We identified significant phenotypic variation in thermal tolerance between populations. Next, to explore whether such variation can be generated by differences in temperature, we conducted an experimental passage study by establishing six replicate lines from a single field-derived population of Ae. aegypti from Mexico, maintaining half at 27°C and the other half at 31°C. After 10 generations, we found a significant difference in mosquito performance, with the lines maintained under elevated temperatures showing greater thermal tolerance. Moreover, these differences in thermal tolerance translated to shifts in the thermal performance curves for multiple life-history traits, leading to differences in overall fitness. Together, these novel findings provide compelling evidence that Ae. aegypti populations can and do differ in thermal response, suggesting that simplified thermal performance models might be insufficient for predicting the effects of climate on vector-borne disease transmission.

Thermal plasticity over a marine-estuarine ecocline can buffer a tropical fish from warming

Intraspecific variation in thermal tolerance can favor species persistence in a warmer ocean, but is often overlooked in fine-scale studies. Nonetheless, local drivers (e.g. salinity) interact with temperature to shape species' thermal response. Here, we acclimated juveniles of Brazilian silversides Atherinella brasiliensis captured at the limits of a marine-estuarine ecocline under reciprocal-cross conditions, to test for phenotypic plasticity in heat tolerance. We also tested whether silversides acclimated to temperatures predicted for 2100 (+3–4.5 °C). Fish in warm-brackish waters showed higher CTMax (Critical Thermal Maximum) than those in cold-marine conditions, regardless of their origin. Silversides’ CTMax reached up to 40.6 °C, but it did not increase after exposure to temperatures predicted for 2100. Lack of acclimation response suggests that silversides heat tolerance has reached a “ceiling”, despite thermal plasticity. Our findings show that fine-scale environmental heterogeneity can promote phenotypic plasticity for tropical species, reducing the risk of short-term extirpation.

Comparative assessment of heat tolerance in weevils associated with a fire‐prone ecosystem

Abstract Fire is an important cause of disturbance which directly shapes many ecosystems worldwide. While the effect of fire on the distribution and regeneration of plant species has been widely documented, little is known on how phytophagous insects are reacting to these disturbances. This study explores the survival strategies of various weevil species, a highly diverse phytophagous beetle group in fire‐prone ecosystems of the biodiversity hotspot of the Cape Floristic Region in South Africa. More specifically, we investigated how the lifestyle of species (location of larval development, phenology of adults, and flight ability) correlates with heat tolerance. We hypothesized that wingless species in particular will show better tolerance to heat as they have a limited ability to escape fire rapidly and usually remain hidden in the soil. The thermal tolerance of a set of sixteen species with divergent lifestyles and geographic distribution was measured using a standard heat knockdown protocol at 48°C. Respirometry was then performed on the most resistant species using a ramping protocol in order to determine CTmax. Our results show that the species tested exhibit high variation in thermal tolerance across taxonomic groups, clustering into three modalities: weak, intermediate, and high tolerance to heat stress. In addition, life history traits (diurnal vs. nocturnal adult activity and location of juvenile stages in plant tissues) likely better explain thermal tolerance at the species level than flight ability or the fire‐proneness of ecosystems. Finally, results revealed that some non‐flying weevil species are highly heat tolerant with CTmax values reaching up to 50.2 and 51.9°C in species among the Ocladiinae and Brachycerinae subfamilies, respectively. Climate change is leading to an increase in the impact and frequency of fires. In this context, this study highlights the diversity of strategies developed by arthropods to escape extreme heat in fire prone ecosystems. Further work is necessary to examine the generality of these patterns across other fire prone ecosystems to better understand behavioural compensation and evolutionary responses, especially given the forecast increases in fire driven by drying and warming associated with climate change.

Greater evolutionary divergence of thermal limits within marine than terrestrial species

There is considerable uncertainty regarding which ecosystems are most vulnerable to warming. Current understanding of organismal sensitivity is largely centred on species-level assessments that do not consider variation across populations. Here we used meta-analysis to quantify upper thermal tolerance variation across 305 populations from 61 terrestrial, freshwater, marine and intertidal taxa. 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 connectivity in the ocean should reduce intraspecific variation. Such adaptive differentiation in the ocean suggests there may be standing genetic variation at the species level to buffer climate impacts. Assessments of vulnerability to warming should account for variation in thermal tolerance among populations (or the lack thereof) to improve predictions about climate vulnerability.

The effects of marine heatwaves on acute heat tolerance in corals.

Scleractinian coral populations are increasingly exposed to conditions above their upper thermal limits due to marine heatwaves, contributing to global declines of coral reef ecosystem health. However, historic mass bleaching events indicate there is considerable inter- and intra-specific variation in thermal tolerance whereby species, individual coral colonies and populations show differential susceptibility to exposure to elevated temperatures. Despite this, we lack a clear understanding of how heat tolerance varies across large contemporary and historical environmental gradients, or the selective pressures that underpin this variation. Here we conducted standardised acute heat stress experiments to identify variation in heat tolerance among species and isolated reefs spanning a large environmental gradient across the Coral Sea Marine Park. We quantified the photochemical yield (Fv /Fm ) of coral samples in three coral species, Acropora cf humilis, Pocillopora meandrina, and Pocillopora verrucosa, following exposure to four temperature treatments (local ambient temperatures, and + 3°C, +6°C and + 9°C above local maximum monthly mean). We quantified the temperature at which Fv /Fm decreased by 50% (termed ED50) and used derived values to directly compare acute heat tolerance across reefs and species. The ED50 for Acropora was 0.4-0.7°C lower than either Pocillopora species, with a 0.3°C difference between the two Pocillopora species. We also recorded 0.9°C to 1.9°C phenotypic variation in heat tolerance among reefs within species, indicating spatial heterogeneity in heat tolerance across broad environmental gradients. Acute heat tolerance had a strong positive relationship to mild heatwave exposure over the past 35 years (since 1986) but was negatively related to recent severe heatwaves (2016-2020). Phenotypic variation associated with mild thermal history in local environments provides supportive evidence that marine heatwaves are selecting for tolerant individuals and populations; however, this adaptive potential may be compromised by the exposure to recent severe heatwaves.

Variation in Thermal Tolerance of the Giant Kelp’s Gametophytes: Suitability of Habitat, Population Quality or Local Adaptation?

The giant kelp Macrocystis pyrifera is a cosmopolitan species of cold-temperate coasts. Its South-American distribution ranges from Peru to Cape Horn and Argentina, encompassing a considerable temperature gradient, from 3 to 20°C. Temperature is known to strongly affect survival, growth and reproduction of many kelp species, and ongoing global warming is already eroding their range distribution. Their response to thermal variability was shown to vary among genetically differentiated regions and populations, suggesting a possible adaptive divergence in thermal tolerance traits. This study aimed at testing the existence of local adaptation in the giant kelp, in regions separated by up to 4000km and strong thermal divergence. Two complementary experiments mimicked reciprocal transplants through a common garden approach, each habitat being represented by a given temperature corresponding to the regional average of the sampled populations. Several proxies of fitness were measured in the haploid stage of the kelp, and sympatric versus allopatric conditions (i.e. individuals at the temperature of their region of origin versus in a different temperature and versus individuals from other regions in that temperature) were compared. Additionally, a heat wave at 24°C was applied to measure the tolerance limits of these gametophytes. A significant interaction between experimental temperature and region of origin revealed that temperature tolerance varied among regions. However, depending on the fitness parameter measured, high latitude populations from the sub-Antarctic region were not always less heat resilient than populations from the warmer region of Peru. Even at 24°C, a temperature that is exceptionally reached in the southernmost part of the kelp’s natural habitat, all the gametophytes survived, although with strong differences in other traits among regions and populations within regions. This large range of temperature tolerance supports the idea of kelp gametophytes being a resistant stage. Finally, local adaptation sensu stricto was not detected. Fertility was more influenced by the geographic origin than by temperature, with possible effects of marginal conditions at the extremes of the distribution range. The latter results also suggest that stochastic dynamics such as genetic drift restricts adaptive processes in some populations of M. pyrifera.

Validating the automation of different measures of high temperature tolerance of small terrestrial insects

Accurately phenotyping numerous test subjects is essential for most experimental research. Collecting such data can be tedious or time-consuming, and it can be biased or limited using manual observations. The thermal tolerance of small ectotherms is a good example of this type of phenotypic data, and it is widely used to investigate thermal adaptation, acclimation capacity and climate change resilience of small ectotherms. Here, we present the results of automatically generated thermal tolerance data using motion-tracking software on video recordings. The automatization was applied to two different heat tolerance assays, in two Drosophila species and used temperature acclimation to create variation in thermal tolerances. We find similar effect sizes of acclimation and hardening responses between manual and automated approaches, but different absolute tolerance estimates. This discrepancy likely reflects both technical differences in the assay conditions as well as the measured end-points of the assays. We conclude that both methods generate biological meaningful results, which reflect different aspects of the thermal biology, find no evidence of inflated variance in the manually scored assays, but find that automation can increase throughput several times without compromising quality. Further we show that the method can be applied to a wide range of arthropod taxa. We suggest that this automated method is a useful example of high throughput phenotyping. Further, we suggest this approach might be applied to other tedious laboratory traits, such as desiccation or starvation tolerance, with similar benefits to throughput but caution that the interpretation and potential comparison to results using different methodology rely on thorough validation of the assay and the involved biological mechanism.

Into the wild-a field study on the evolutionary and ecological importance of thermal plasticity in ectotherms across temperate and tropical regions.

Understanding how environmental factors affect the thermal tolerance of species is crucial for predicting the impact of thermal stress on species abundance and distribution. To date, species' responses to thermal stress are typically assessed on laboratory-reared individuals and using coarse, low-resolution, climate data that may not reflect microhabitat dynamics at a relevant scale. Here, we examine the daily temporal variation in heat tolerance in a range of species in their natural environments across temperate and tropical Australia. Individuals were collected in their habitats throughout the day and tested for heat tolerance immediately thereafter, while local microclimates were recorded at the collection sites. We found high levels of plasticity in heat tolerance across all the tested species. Both short- and long-term variability of temperature and humidity affected plastic adjustments of heat tolerance within and across days, but with species differences. Our results reveal that plastic changes in heat tolerance occur rapidly at a daily scale and that environmental factors on a relatively short timescale are important drivers of the observed variation in thermal tolerance. Ignoring such fine-scale physiological processes in distribution models might obscure conclusions about species' range shifts with global climate change. This article is part of the theme issue 'Species' ranges in the face of changing environments (part 1)'.

No consistent effect of daytime versus night-time measurement of thermal tolerance in nocturnal and diurnal lizards.

While essential in understanding impacts of climate change for organisms, diel variation remains an understudied component of temporal variation in thermal tolerance limits [i.e. the critical thermal minimum (CTmin) and maximum (CTmax)]. For example, a higher Ctmax might be expected for an individual if the measurement is taken during the day (when heat stress is most likely to occur) instead of at night. We measured thermal tolerance (Ctmin and Ctmax) during both the daytime and night-time in 101 nocturnal and diurnal geckos and skinks in Hong Kong and in South Africa, representing six species and covering a range of habitats. We found that period of measurement (day vs. night) only affected Ctmin in South Africa (but not in Hong Kong) and that Ctmax was unaffected. Body size and species were important factors for determining Ctmax in Hong Kong and Ctmin in South Africa, respectively. Overall, however, we did not find consistent diel variation of thermal tolerance and suggest that measurements of critical thermal limits may be influenced by timing of measurement-but that such effects, when present, are likely to be context-dependent.

Intraspecific variation in thermal tolerance differs between tropical and temperate fishes

How ectothermic animals will cope with global warming is a critical determinant of the ecological impacts of climate change. There has been extensive study of upper thermal tolerance limits among fish species but how intraspecific variation in tolerance may be affected by habitat characteristics and evolutionary history has not been considered. Intraspecific variation is a primary determinant of species vulnerability to climate change, with implications for global patterns of impacts of ongoing warming. Using published critical thermal maximum (CTmax) data on 203 fish species, we found that intraspecific variation in upper thermal tolerance varies according to a species’ latitude and evolutionary history. Overall, tropical species show a lower intraspecific variation in thermal tolerance than temperate species. Notably, freshwater tropical species have a lower variation in tolerance than freshwater temperate species, which implies increased vulnerability to impacts of thermal stress. The extent of variation in CTmax among fish species has a strong phylogenetic signal, which may indicate a constraint on evolvability to rising temperatures in tropical fishes. That is, in addition to living closer to their upper thermal limits, tropical species may have higher sensitivity and lower adaptability to global warming compared to temperate counterparts. This is evidence that freshwater tropical fish communities, worldwide, are especially vulnerable to ongoing climate change.

Phytoplankton biodiversity is more important for ecosystem functioning in highly variable thermal environments

The 21st century has seen an acceleration of anthropogenic climate change and biodiversity loss, with both stressors deemed to affect ecosystem functioning. However, we know little about the interactive effects of both stressors and in particular about the interaction of increased climatic variability and biodiversity loss on ecosystem functioning. This should be remedied because larger climatic variability is one of the main features of climate change. Here, we demonstrated that temperature fluctuations led to changes in the importance of biodiversity for ecosystem functioning. We used microcosm communities of different phytoplankton species richness and exposed them to a constant, mild, and severe temperature-fluctuating environment. Wider temperature fluctuations led to steeper biodiversity-ecosystem functioning slopes, meaning that species loss had a stronger negative effect on ecosystem functioning in more fluctuating environments. For severe temperature fluctuations, the slope increased through time due to a decrease of the productivity of species-poor communities over time. We developed a theoretical competition model to better understand our experimental results and showed that larger differences in thermal tolerances across species led to steeper biodiversity-ecosystem functioning slopes. Species-rich communities maintained their ecosystem functioning with increased fluctuation as they contained species able to resist the thermally fluctuating environments, while this was on average not the case in species-poor communities. Our results highlight the importance of biodiversity for maintaining ecosystem functions and services in the context of increased climatic variability under climate change.

How will mosquitoes adapt to climate warming?

The potential for adaptive evolution to enable species persistence under a changing climate is one of the most important questions for understanding impacts of future climate change. Climate adaptation may be particularly likely for short-lived ectotherms, including many pest, pathogen, and vector species. For these taxa, estimating climate adaptive potential is critical for accurate predictive modeling and public health preparedness. Here, we demonstrate how a simple theoretical framework used in conservation biology—evolutionary rescue models—can be used to investigate the potential for climate adaptation in these taxa, using mosquito thermal adaptation as a focal case. Synthesizing current evidence, we find that short mosquito generation times, high population growth rates, and strong temperature-imposed selection favor thermal adaptation. However, knowledge gaps about the extent of phenotypic and genotypic variation in thermal tolerance within mosquito populations, the environmental sensitivity of selection, and the role of phenotypic plasticity constrain our ability to make more precise estimates. We describe how common garden and selection experiments can be used to fill these data gaps. Lastly, we investigate the consequences of mosquito climate adaptation on disease transmission using Aedes aegypti-transmitted dengue virus in Northern Brazil as a case study. The approach outlined here can be applied to any disease vector or pest species and type of environmental change.

Choosing source populations for conservation reintroductions: lessons from variation in thermal tolerance among populations of the imperilled redside dace1

Reintroduction is an increasingly common conservation tool used to recover populations of imperilled species, but its success depends on the suitability of the introduced animals’ phenotype for their new habitat. For fishes, thermal tolerance may be a key trait in urbanized habitats. We compared thermal tolerance (CTmax) among three lineages (western, central, eastern) of imperilled redside dace (Clinostomus elongatus). CTmax of eastern adults was 3–4 °C lower than that of the other lineages, but adults of each lineage had similar thermal acclimation responses. In contrast, the acclimation response of juveniles differed by ∼80% between the central and western lineages. Using these data, we predicted how each lineage would fare in a hypothetical reintroduction to relatively warm urbanized habitats. Owing to the differences in juvenile acclimation responses, predicted thermal safety margins for the central lineage were double those predicted for the western lineage. Overall, we suggest that CTmax is a useful trait to incorporate into the source population selection process; however, there is an urgent need for the establishment of captive experimental research populations of imperilled species to address remaining uncertainties.

Does geographic variation in thermal tolerance in Daphnia represent trade-offs or conditional neutrality?

Geographic variation in thermal tolerance in Daphnia seems to represent genetic load at the loci specifically responsible for heat tolerance resulting from conditional neutrality. We see no evidence of trade-offs between fitness-related traits at 25°C vs. 10 °C or between two algal diets across Daphnia magna clones from a variety of locations representing the opposite ends of the distribution of long-term heat tolerance. Likewise, we found no evidence of within-environment trade-offs between heat tolerance and fitness-related traits in any of the environments. Neither short-term and long-term heat tolerance shows any consistent relationship with lipid fluorescence polarization and lipid peroxidation across clones or environments. Pervasive positive correlations between fitness-related traits indicate differences in genetic load rather than trade-off based local adaptation or thermal specialization. For heat tolerance such differences may be caused by either relaxation of stabilizing selection due to lower exposure to high temperature extremes, i.e., conditional neutrality, or by small effective population size followed by the recent range expansion.

Climate vulnerability of South American freshwater fish: Thermal tolerance and acclimation.

Freshwater fish are restricted by their physiology to rivers and lakes, and are generally limited in their capacity to disperse across basins. As a result, there is often a close match between the evolutionary history of river basins and their natural history. Thus, the regional landscape and ecological features, such as temperature, have shaped the evolution and adaptation of local fish assemblages. Climate change is expected to affect fish diversity and increase extinction, especially in low latitudes, and it has been suggested that species that inhabit low latitude species are more susceptible since they live close to their maximum thermal limits and have low capacity for acclimation. To understand the mechanisms of variation in thermal tolerance across a broad-scale of South American fishes is fundamental to be able to assess the vulnerability of species and habitat to global warming. Herein, we present the first attempt to analyze the vulnerability of South American freshwater fish species, based on the review of upper thermal limits of 106 species from a broad range of latitudinal habitats. Our findings show that upper thermal limits decrease with latitude, while the thermal safety margin (TSM) increase. Furthermore, the latitude has little effects on the acclimation response ratio, and the TSM decreased with rising temperatures. These data suggest that thermal phenotypic acclimation has low potential for mitigating global warming. These results indicate that South American fish species living in tropical areas are more susceptible to global warming since they are already living close to their maximum habitat temperature.

The evolution of critical thermal limits of life on Earth

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary ‘attractors’ that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.