Differential response to heat stress among evolutionary lineages of an aquatic invertebrate species complex (original) (raw)
Related papers
Greater evolutionary divergence of thermal limits within marine than terrestrial species
Nature Climate Change, 2022
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 intraspeci c variation. Our ndings 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.
PLOS ONE, 2019
Genetic divergence is impacted by many factors, including phylogenetic history, gene flow, genetic drift, and divergent selection. Rotifers are an important component of aquatic ecosystems, and genetic variation is essential to their ongoing adaptive diversification and local adaptation. In addition to coding sequence divergence, variation in gene expression may relate to variable heat tolerance, and can impose ecological barriers within species. Temperature plays a significant role in aquatic ecosystems by affecting species abundance, spatio-temporal distribution, and habitat colonization. Recently described (formerly cryptic) species of the Brachionus calyciflorus complex exhibit different temperature tolerance both in natural and in laboratory studies, and show that B. calyciflorus sensu stricto (s.s.) is a thermotolerant species. Even within B. calyciflorus s.s., there is a tendency for further temperature specializations. Comparison of expressed genes allows us to assess the impact of stressors on both expression and sequence divergence among disparate populations within a single species. Here, we have used RNA-seq to explore expressed genetic diversity in B. calyciflorus s.s. in two mitochondrial DNA lineages with different phylogenetic histories and differences in thermotolerance. We identify a suite of candidate genes that may underlie local adaptation, with a particular focus on the response to sustained high or low temperatures. We do not find adaptive divergence in established candidate genes for thermal adaptation. Rather, we detect divergent selection among our two lineages in genes related to metabolism (lipid metabolism, metabolism of xenobiotics).
Functional Ecology, 2012
1. 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. 2. 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. 3. 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. 4. 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. 5. 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.
GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms
Scientific data, 2018
How climate affects species distributions is a longstanding question receiving renewed interest owing to the need to predict the impacts of global warming on biodiversity. Is climate change forcing species to live near their critical thermal limits? Are these limits likely to change through natural selection? These and other important questions can be addressed with models relating geographical distributions of species with climate data, but inferences made with these models are highly contingent on non-climatic factors such as biotic interactions. Improved understanding of climate change effects on species will require extensive analysis of thermal physiological traits, but such data are both scarce and scattered. To overcome current limitations, we created the GlobTherm database. The database contains experimentally derived species' thermal tolerance data currently comprising over 2,000 species of terrestrial, freshwater, intertidal and marine multicellular algae, plants, fung...
Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits
2005
Temperature-adaptive physiological variation plays important roles in latitudinal biogeographic patterning and in setting vertical distributions along subtidal-to-intertidal gradients in coastal marine ecosystems. Comparisons of congeneric marine invertebrates reveal that the most warm-adapted species may live closer to their thermal tolerance limits and have lower abilities to increase heat tolerance through acclimation than more cold-adapted species. In crabs and snails, heart function may be of critical importance in establishing thermal tolerance limits. Temperature-mediated shifts in gene expression may be critical in thermal acclimation. Transcriptional changes, monitored using cDNA microarrays, have been shown to differ between steady-state thermal acclimation and diurnal temperature cycling in a eurythermal teleost fish (Austrofundulus limnaeus). In stenothermal Antarctic notothenioid fish, losses in capacity for temperature-mediated gene expression, including the absence of a heat-shock response, may reduce the abilities of these species to acclimate to increased temperatures. Differences among species in thermal tolerance limits and in the capacities to adjust these limits may determine how organisms are affected by climate change.
Journal of Experimental Biology, 2010
SUMMARY Physiological studies can help predict effects of climate change through determining which species currently live closest to their upper thermal tolerance limits, which physiological systems set these limits, and how species differ in acclimatization capacities for modifying their thermal tolerances. Reductionist studies at the molecular level can contribute to this analysis by revealing how much change in sequence is needed to adapt proteins to warmer temperatures — thus providing insights into potential rates of adaptive evolution — and determining how the contents of genomes — protein-coding genes and gene regulatory mechanisms — influence capacities for adapting to acute and long-term increases in temperature. Studies of congeneric invertebrates from thermally stressful rocky intertidal habitats have shown that warm-adapted congeners are most susceptible to local extinctions because their acute upper thermal limits (LT50 values) lie near current thermal maxima and their ...
Global change biology, 2015
Predicting species vulnerability to global warming requires a comprehensive, mechanistic understanding of sublethal and lethal thermal tolerances. To date, however, most studies investigating species physiological responses to increasing temperature have focused on the underlying physiological traits of either acute or chronic tolerance in isolation. Here we propose an integrative, synthetic approach including the investigation of multiple physiological traits (metabolic performance and thermal tolerance), and their plasticity, to provide more accurate and balanced predictions on species and assemblage vulnerability to both acute and chronic effects of global warming. We applied this approach to more accurately elucidate relative species vulnerability to warming within an assemblage of six caridean prawns occurring in the same geographic, hence macroclimatic, region, but living in different thermal habitats. Prawns were exposed to four incubation temperatures (10, 15, 20 and 25 °C) ...
Biological Journal of the Linnean Society, 2014
Considerable attention has been given to the potential impacts of global climate change on biodiversity. In the present study, we combine understudied themes by examining the ability of a freshwater fish (polymorphic for heat-sensitivity) to respond to short-term thermal stress mimicking an extreme temperature event. We simultaneously measured the effect of thermal stress on the body condition of heat-sensitive and heat-tolerant forms to evaluate an existing hypothesis regarding the underlying mechanism by which temperature affects the maintenance of genetic variation in this species. Surprisingly, the heat-sensitive allelic variant increased in body condition equally as much as a heat-tolerant variant under acute heat stress. More importantly, the heat-sensitive variant exhibited a significant response to thermal stress, with an upward shift of greater than 2°C in critical thermal maximum. Our findings suggest a complexity to the relationship between thermal stress and male body condition that may depend on an interaction with other factors such as resource level. Although the evolutionary fate of species with respect to climate change is typically evaluated in terms long-term adaptive response, short-term selection events could drastically reduce fitness and reduce evolutionary potential. Our results suggest that heat-sensitive species may have considerably greater resilience to the short-term, extreme perturbations to the environment that are expected under climate change.
Scientific Reports
The impact of climate change on biodiversity has stimulated the need to understand environmental stress responses, particularly for ecosystem engineers whose responses to climate affect large numbers of associated organisms. Distinct species differ substantially in their resilience to thermal stress but there are also within-species variations in thermal tolerance for which the molecular mechanisms underpinning such variation remain largely unclear. Intertidal mussels are well-known for their role as ecosystem engineers. First, we exposed two genetic lineages of the intertidal mussel Perna perna to heat stress treatments in air and water. Next, we ran a high throughput RNA sequencing experiment to identify differences in gene expression between the thermally resilient eastern lineage and the thermally sensitive western lineage. We highlight different thermal tolerances that concord with their distributional ranges. Critically, we also identified lineage-specific patterns of gene exp...
Global cooling as a driver of diversification in a major marine clade
Nature Communications, 2016
Climate is a strong driver of global diversity and will become increasingly important as human influences drive temperature changes at unprecedented rates. Here we investigate diversification and speciation trends within a diverse group of aquatic crustaceans, the Anomura. We use a phylogenetic framework to demonstrate that speciation rate is correlated with global cooling across the entire tree, in contrast to previous studies. Additionally, we find that marine clades continue to show evidence of increased speciation rates with cooler global temperatures, while the single freshwater clade shows the opposite trend with speciation rates positively correlated to global warming. Our findings suggest that both global cooling and warming lead to diversification and that habitat plays a role in the responses of species to climate change. These results have important implications for our understanding of how extant biota respond to ongoing climate change and are of particular importance fo...