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Synopsis The presence of standing genetic variation will play a role in determining a population's capacity to adapt to environmentally relevant stressors. In the Gulf of Mexico, extreme climatic events and anthropogenic changes to local hydrology will expose productive oyster breeding grounds to stressful low salinity conditions. We identified genetic variation for performance under low salinity (due to the combined effects of low salinity and genetic load) using a single-generation selection experiment on larvae from two populations of the eastern oyster, Crassostrea virginica. We used pool-sequencing to test for allele frequency differences at 152 salinity-associated genes for larval families pre- and post-low salinity exposure. Our results have implications for how evolutionary change occurs during early life history stages at environmentally relevant salinities. Consistent with observations of high genetic load observed in oysters, we demonstrate evidence for purging of deleterious alleles at the larval stage in C. virginica. In addition, we observe increases in allele frequencies at multiple loci, suggesting that natural selection for low salinity performance at the larval stage can act as a filter for genotypes found in adult populations.

Rapid evolution may provide a buffer against extinction risk for some species threatened by climate change; however, the capacity to evolve rapidly enough to keep pace with changing environments is unknown for most taxa. The ecosystem-level consequences of climate adaptation are likely to be the largest in marine ecosystems, where short-lived phytoplankton with large effective population sizes make up the bulk of primary production. However, there are substantial challenges to predicting climate-driven evolution in marine systems, including multiple simultaneous axes of change and considerable heterogeneity in rates of change, as well as the biphasic life cycles of many marine metazoans, which expose different life stages to disparate sources of selection. A critical tool for addressing these challenges is experimental evolution, where populations of organisms are directly exposed to controlled sources of selection to test evolutionary responses. We review the use of experimental evolution to test the capacity to adapt to climate change stressors in marine species. The application of experimental evolution in this context has grown dramatically in the past decade, shedding light on the capacity for evolution, associated trade-offs, and the genetic architecture of stress-tolerance traits. Our goal is to highlight the utility of this approach for investigating potential responses to climate change and point a way forward for future studies.

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.

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.

The eastern oyster, Crassostrea virginica, forms reefs that provide critical services to the surrounding ecosystem. These reefs are at risk from climate change, in part because altered rainfall patterns may amplify local fluctuations in salinity, impacting oyster recruitment, survival, and growth. As in other marine organisms, warming water temperatures might interact with these changes in salinity to synergistically influence oyster physiology. In this study, we used comparative transcriptomics, measurements of physiology, and a field assessment to investigate what phenotypic changes C. virginica uses to cope with combined temperature and salinity stress in the Gulf of Mexico. Oysters from a historically low salinity site (Sister Lake, LA) were exposed to fully crossed temperature (20°C and 30°C) and salinity (25, 15, and 7 PSU) treatments. Using comparative transcriptomics on oyster gill tissue, we identified a greater number of genes that were differentially expressed (DE) in response to low salinity at warmer temperatures. Functional enrichment analysis showed low overlap between genes DE in response to thermal stress compared with hypoosmotic stress and identified enrichment for gene ontologies associated with cell adhesion, transmembrane transport, and microtubule-based process. Experiments also showed that oysters changed their physiology at elevated temperatures and lowered salinity, with significantly increased respiration rates between 20°C and 30°C. However, despite the higher energetic demands, oysters did not increase their feeding rate. To investigate transcriptional differences between populations in situ, we collected gill tissue from three locations and two time points across the Louisiana Gulf coast and used quantitative PCR to measure the expression levels of seven target genes. We found an upregulation of genes that function in osmolyte transport, oxidative stress mediation, apoptosis, and protein synthesis at our low salinity site and sampling time point. In summary, oysters altered their phenotype more in response to low salinity at higher temperatures as evidenced by a higher number of DE genes during laboratory exposure, increased respiration (higher energetic demands), and in situ differential expression by season and location. These synergistic effects of hypoosmotic stress and increased temperature suggest that climate change will exacerbate the negative effects of low salinity exposure on eastern oysters.

As species struggle to keep pace with the rapidly warming climate, adaptive introgression of beneficial alleles from closely related species or populations provides a possible avenue for rapid adaptation. We investigate the potential for adaptive introgression in the copepod, Tigriopus californicus, by hybridizing two populations with divergent heat tolerance limits. We subjected hybrids to strong heat selection for 15 generations followed by whole-genome resequencing. Utilizing a hybridize evolve and resequence (HER) technique, we can identify loci responding to heat selection via a change in allele frequency. We successfully increased the heat tolerance (measured as LT50) in selected lines, which was coupled with higher frequencies of alleles from the southern (heat tolerant) population. These repeatable changes in allele frequencies occurred on all 12 chromosomes across all independent selected lines, providing evidence that heat tolerance is polygenic. These loci contained genes with lower protein-coding sequence divergence than the genome-wide average, indicating that these loci are highly conserved between the two populations. In addition, these loci were enriched in genes that changed expression patterns between selected and control lines in response to a nonlethal heat shock. Therefore, we hypothesize that the mechanism of heat tolerance divergence is explained by differential gene expression of highly conserved genes. The HER approach offers a unique solution to identifying genetic variants contributing to polygenic traits, especially variants that might be missed through other population genomic approaches.

The eastern oyster, Crassostrea virginica, is a foundation species within US Gulf of Mexico (GoM) estuaries that has experienced substantial population declines. As changes from management and climate are expected to continue to impact estuarine salinity, understanding how local oyster populations might respond and identifying populations with adaptations to more extreme changes in salinity could inform resource management, including restoration and aquaculture programs. Wild oysters were collected from four estuarine sites from Texas [Packery Channel (PC): 35.5, annual mean salinity, Aransas Bay (AB): 23.0] and Louisiana [Calcasieu Lake (CL): 16.2, Vermilion Bay (VB): 7.4] and spawned. The progeny were compared in field and laboratory studies under different salinity regimes. For the field study, F1 oysters were deployed at low (6.4) and intermediate (16.5) salinity sites in Alabama. Growth and mortality were measured monthly. Condition index and Perkinsus marinus infection intensity were measured quarterly. For the laboratory studies, mortality was recorded in F1 oysters that were exposed to salinities of 2.0, 4.0, 20.0/22.0, 38.0 and 44.0 with and without acclimation. The results of the field study and laboratory study with acclimation indicated that PC oysters are adapted to high-salinity conditions and do not tolerate very low salinities. The AB stock had the highest plasticity as it performed as well as the PC stock at high salinities and as well as Louisiana stocks at the lowest salinity. Louisiana stocks did not perform as well as the Texas stocks at high salinities. Results from the laboratory studies without salinity acclimation showed that all F1 stocks experiencing rapid mortality at low salinities when 3-month oysters collected at a salinity of 24 were used and at both low and high salinities when 7-month oysters collected at a salinity of 14.5 were used.

Neophobia (aversion to new objects, food, and environments) is a personality trait that affects the ability of wildlife to adapt to new challenges and opportunities. Despite the ubiquity and importance of this trait, the molecular mechanisms underlying repeatable individual differences in neophobia in wild animals are poorly understood. We evaluated wild-caught house sparrows (Passer domesticus) for neophobia in the lab using novel object tests. We then selected the most and least neophobic individuals (n=3 of each) and extracted RNA from four brain regions involved in learning, memory, threat perception, and executive function: striatum, dorsomedial hippocampus, medial ventral arcopallium, and caudolateral nidopallium (NCL). Our analysis of differentially expressed genes (DEGs) used 11,889 gene regions annotated in the house sparrow reference genome for which we had an average of 25.7 million mapped reads/sample. PERMANOVA identified significant effects of brain region, phenotype (neophobic vs. non-neophobic), and a brain region by phenotype interaction. Comparing neophobic and non-neophobic birds revealed constitutive differences in DEGs in three of the four brain regions examined: hippocampus (12% of the transcriptome significantly differentially expressed), striatum (4%) and NCL (3%). DEGs included important known neuroendocrine mediators of learning, memory, executive function, and anxiety behavior, including serotonin receptor 5A, dopamine receptors 1, 2 and 5 (downregulated in neophobic birds), and estrogen receptor beta (upregulated in neophobic birds). These results suggest that some of the behavioral differences between phenotypes may be due to underlying gene expression differences in the brain. The large number of DEGs in neophobic and non-neophobic birds also implies that there are major differences in neural function between the two phenotypes that could affect a wide variety of behavioral traits beyond neophobia.

Eastern oysters in the northern Gulf of Mexico are routinely infected with the protistan parasite Perkinsus marinus, the cause of the disease commonly known as dermo. Recent experimental challenges among Atlantic coast populations have identified both resistant and susceptible genotypes using comparative transcriptomics. While controlled experimental challenges are essential first assessments, expanding this analysis to field reared individuals provides an opportunity to identify key genomic signatures of infection that appear both in the laboratory and in the field. In this study we combined reduced representation bisulfite sequencing with 3′ RNA sequencing (Tag-seq) to describe two molecular phenotypes associated with infection in oysters outplanted at a common garden field site. These combined approaches allowed us to examine changes in DNA methylation and gene expression for a large number of individuals (n = 40) that developed infections during the course of a common garden outplant experiment. Our epigenetic analysis of DNA methylation identified significant changes in gene body methylation associated with increasing infection intensity, across genes associated with immune responses. There was a smaller transcriptomic response to increasing infection intensities with 32 genes showing differential expression; however, only 40% of these genes were found to also be differentially methylated. While there was no clear pattern between direction of differential methylation and gene expression, there was a significant effect of percent methylation on gene-by-gene expression levels and the coefficient of variation in gene body methylation between treatments. These results show that in C. virginica, heavily methylated genes have high levels of gene expression with low levels of variation. Comparing our differential expression results with previously published experimental P. marinus challenges identified overlapping expression patterns for genes associated with C1q-domain-containing and V-type proton ATPase proteins. Through our comparative transcriptomic approach using field reared individuals and co-expression network analysis we have also been able to identify a network of genes that change in expression in response to infection. These combined analyses provide evidence for a conserved response to P. marinus infections across infection intensities and suggest that DNA methylation may not be a reliable predictor of differential gene expression in long-term infections.

Understanding the mechanisms with which organisms can respond to a rapidly changing ocean is an important research priority in marine sciences, especially in the light of recent predictions regarding the pace of ocean change in the coming decades. Transgenerational effects, in which the experience of the parental generation can shape the phenotype of their offspring, may serve as such a mechanism. In this study, adult purple sea urchins, Strongylocentrotus purpuratus, were conditioned to regionally and ecologically relevant pCO2 levels and temperatures representative of upwelling (colder temperature and high pCO2 ) and nonupwelling (average temperature and low pCO2 ) conditions typical of coastal upwelling regions in the California Current System. Following 4.5 months of conditioning, adults were spawned and offspring were raised under either high or low pCO2 levels, to examine the role of maternal effects. Using RNA-seq and comparative transcriptomics, our results indicate that differential conditioning of the adults had an effect on the gene expression patterns of the progeny during the gastrula stage of early development. For example, maternal conditioning under upwelling conditions intensified the transcriptomic response of the progeny when they were raised under high versus low pCO2 conditions. Additionally, mothers that experienced upwelling conditions produced larger progeny. The overall findings of this study are complex, but do suggest that transgenerational plasticity in situ could act as an important mechanism by which populations might keep pace with rapid environmental change.

Thinking about the evolutionary causes and consequences of trait correlations has been dominated by quantitative genetics theory that is focused on hypothetical loci. Since this theory was initially developed, technology has enabled the identification of specific genetic variants that contribute to trait correlations. Here, we review studies of the genetic basis of trait correlations to ask: What has this new information taught us? We find that causal variants can be pleiotropic and/or linked in different ways, indicating that pleiotropy and linkage are not alternative genetic mechanisms. Further, many trait correlations have a polygenic basis, suggesting that both pleiotropy and linkage likely contribute. We discuss implications of these findings for the evolutionary causes and consequences of trait correlations.

Salinity conditions in oyster breeding grounds in the Gulf of Mexico are expected to drastically change due to increased precipitation from climate change and anthropogenic changes to local hydrology. We determined the capacity of the eastern oyster, Crassostrea virginica , to adapt via standing genetic variation or acclimate through transgenerational plasticity (TGP). We outplanted oysters to either a low- or medium-salinity site in Louisiana for 2 years. We then crossed adult parents using a North Carolina II breeding design, and measured body size and survival of larvae 5 dpf raised under low or ambient salinity. We found that TGP is unlikely to significantly contribute to low-salinity tolerance since we did not observe increased growth or survival in offspring reared in low salinity when their parents were also acclimated at a low-salinity site. However, we detected genetic variation for body size, with an estimated heritability of 0.68 ± 0.25 (95% CI). This suggests there is ample genetic variation for this trait to evolve, and that evolutionary adaptation is a possible mechanism through which oysters will persist with future declines in salinity. The results of this experiment provide valuable insights into successfully breeding low-salinity tolerance in this commercially important species.

Summary 1.Organisms may respond to changing environments through phenotypic plasticity or adaptive evolution. These two processes are not mutually exclusive, and may either dampen or strengthen each other's effects, depending on the genetic correlation between trait values and the slopes of their norms of reaction. 2.To examine the effect of adaptation to heat stress on the plasticity of heat tolerance we hybridized populations of the crustacean Tigriopus californicus that show divergent phenotypes for heat tolerance. We then selected for increased heat tolerance in hybrids and measured heat tolerance and the phenotypic plasticity of heat tolerance in both selected lines and unselected controls. 3.To test whether changes in phenotypic plasticity were associated with changes in the plasticity of gene expression, we also sequenced transcriptomes of selected and unselected lines, both under heat shock and at ambient temperatures. 4.We observed increased heat tolerance in selected lines, but also lower phenotypic and transcriptional plasticity in response to heat stress. The plastic response to heat stress was highly enriched for hydrolytic and catalytic activities, suggesting a prominent role for degradation of mis-folded proteins. 5.Our findings have important implications for biological responses to climate change: if adaptation to environmental stress reduces plasticity, then plasticity and adaptive evolution will make overlapping, rather than additive contributions to buffering populations from environmental change. This article is protected by copyright. All rights reserved.

Trade‐offs may influence both physiological and evolutionary responses to co‐occurring stressors, but their effects on both plastic and adaptive responses to climate change are poorly understood. To test for genetic and physiological trade‐offs incurred in tolerating multiple stressors, we hybridized two populations of the intertidal copepod Tigriopus californicus that were divergent for both heat and salinity tolerance. Starting in the F2 generation, we selected for increased tolerance of heat, low salinity, and high salinity in replicate lines. After five generations of selection, heat‐selected lines had greater heat tolerance but lower fecundity, indicating an energetic cost to tolerance. Lines selected for increased salinity tolerance did not show evidence of adaptation to their respective environments; however, hypo‐osmotic selection lines showed substantial loss of tolerance to hyperosmotic stress. Neither of the salinity selection regimes resulted in diminished heat tolerance at ambient salinity; however, simultaneous exposure to heat and hypo‐osmotic stress led to decreased heat tolerance, implying a physiological trade‐off in tolerance to the two stressors. When we quantified the transcriptomic response to heat and salinity stress via RNA sequencing, we observed little overlap in the stress responses, suggesting the observed synergistic effects of heat and salinity stress were driven by competing energetic demands, rather than shared stress response pathways.

Physiological plasticity and adaptive evolution may facilitate persistence in a changing environment. As a result, there is an interest in understanding species' capacities for plastic and evolved responses, and the mechanisms by which these responses occur. Transcriptome sequencing has become a powerful tool for addressing these questions, providing insight into otherwise unobserved effects of changing conditions on organismal physiology and variation in these effects among individuals and populations. Here, we review recent studies using comparative transcriptomics to understand plastic and evolutionary responses to changing environments. We focus on 2 areas where transcriptomics has played an important role: first, in understanding the genetic basis for local adaptation to current gradients as a proxy for future adaptation, and second, in understanding organismal responses to multiple stressors. We find most studies examining multiple stressors have tested the effects of each stressor individually; the few studies testing multiple stressors simultaneously have found synergistic effects on gene expression that would not have been predicted from single stressor studies. We discuss the importance of robust experimental design to allow for a more sophisticated characterization of transcriptomic responses and conclude by offering recommendations for future research, including integrating genomics with transcriptomics, testing gene regulatory networks, and comparing the equivalence of transcription to translation and the effects of environmental stress on the proteome.

Many studies have reported reductions in body size and calcification rates for marine larvae exposed to ocean acidification conditions. However, the physiological mechanisms driving these effects, and mechanisms underlying body size variation in general, are poorly understood. Here, we combine transcriptome sequencing with bulked segregant analysis to assess the physiological response to acidification in larvae of the California mussel, Mytilus californianus, and to explore physiological basis of variation in larval size. We reared three families of M. californianus larvae under ambient (∼350 µatm, pHtotal 8.1) and high (∼1300 µatm, pHtotal 7.6) pCO2 conditions, then passed larvae through a mesh filter, separating each family × pCO2 treatment into fractions of larvae with large vs. small body sizes. We sequenced larval mRNA for each family × treatment × body size combination, and assembled a de novo transcriptome. We then mapped reads from each library to this assembly to identify effects of high pCO2 on gene expression, and to identify transcriptomic differences between small vs. large larvae of the same age class. Although larvae reared under elevated pCO2 were smaller, we observed no consistent effect of elevated pCO2 on gene expression. Nevertheless, 1225 transcripts, primarily related to metabolism, were differentially expressed between large vs. small larvae, regardless of CO2 treatment. We conclude that the observed reduction in larval body size under high CO2 may be driven by a direct effect of the environment on phenotype, unmediated by changes in gene expression. Because M. calfornianus has evolved in the context of seasonal upwelling, exposure to 1300 µatm, pCO2 may not produce the large stress-mediated effects on gene expression that might be expected for an organism exposed to conditions far outside those of its typical environment.

Advances in nucleic acid sequencing technology are removing obstacles that historically prevented use of genomics within ocean change biology. As one of the first marine calcifiers to have its genome sequenced, purple sea urchins (Strongylocentrotus purpuratus) have been the subject of early research exploring genomic responses to ocean acidification, work that points to future experiments and illustrates the value of expanding genomic resources to other marine organisms in this new 'post-genomic' era. This review presents case studies of S. purpuratus demonstrating the ability of genomic experiments to address major knowledge gaps within ocean acidification. Ocean acidification research has focused largely on species vulnerability, and studies exploring mechanistic bases of tolerance toward low pH seawater are comparatively few. Transcriptomic responses to high pCO₂ seawater in a population of urchins already encountering low pH conditions have cast light on traits required for success in future oceans. Secondly, there is relatively little information on whether marine organisms possess the capacity to adapt to oceans progressively decreasing in pH. Genomics offers powerful methods to investigate evolutionary responses to ocean acidification and recent work in S. purpuratus has identified genes under selection in acidified seawater. Finally, relatively few ocean acidification experiments investigate how shifts in seawater pH combine with other environmental factors to influence organism performance. In S. purpuratus, transcriptomics has provided insight into physiological responses of urchins exposed simultaneously to warmer and more acidic seawater. Collectively, these data support that similar breakthroughs will occur as genomic resources are developed for other marine species.

The copepod species, Tigriopus californicus, is one of the most thermally adaptable species in the biosphere. They have been found in tide pools from the coast of Alaska down to the coast of Southern California. However, as all other organisms have limits, the T. californicus are only able to tolerate temperatures up to 34oC. By comparing gene expression between specimens exposed to high temperatures and those expressed to optimal temperatures, we identified the genes responsible for conferring tolerance to increasing temperatures. After testing gene expression between copepods at 20oC and at 34oC, we have determined that both the hsp70 gene and the toll-like receptors of the T. californicus play a role in tolerance to temperature variance. L’espece copepode, Tigriopus californicus, est une des especes les plus thermiquement adaptables de la biosphere. On les trouve dans les bâches depuis la cote de l’Alaska jusqu’a la cote sud de la Californie. Toutefois, comme tous les autres organ¬ismes, les Tigriopus californicus ont des limites et ne peuvent pas tolerer des temperatures superieures a 34oC. En comparant l’expression genetique entre les specimens exposes a des temperatures elevees et ceux exposes a des temperatures optimales, nous avons identifie les genes responsables de la tolerance a des temperatures en hausse. Apres avoir teste l’expression genetique entre les copepodes a 20oC et a 34oC, nous avons determine que le gene hsp70 et les recepteurs de type Toll du T. californicus jouent tous deux un role dans la tolerance aux variations de temperature.

Theory suggests that evolutionary changes in phenotypic plasticity could either hinder or facilitate evolutionary rescue in a changing climate. Nevertheless, the actual role of evolving plasticity in the responses of natural populations to climate change remains unresolved. Direct observations of evolutionary change in nature are rare, making it difficult to assess the relative contributions of changes in trait means versus changes in plasticity to climate change responses. To address this gap, this review explores several proxies that can be used to understand evolving plasticity in the context of climate change, including space for time substitutions, experimental evolution and tests for genomic divergence at environmentally responsive loci. Comparisons among populations indicate a prominent role for divergence in environmentally responsive traits in local adaptation to climatic gradients. Moreover, genomic comparisons among such populations have identified pervasive divergence in the regulatory regions of environmentally responsive loci. Taken together, these lines of evidence suggest that divergence in plasticity plays a prominent role in adaptation to climatic gradients over space, indicating that evolving plasticity is also likely to play a key role in adaptive responses to climate change through time. This suggests that genetic variation in plastic responses to the environment (G × E) might be an important predictor of species' vulnerabilities to climate-driven decline or extinction.This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.

Antagonistic correlations among traits may slow the rate of adaptation to a changing environment. The tide pool copepod Tigriopus californicus is locally adapted to temperature, but within populations, the response to selection for increased heat tolerance plateaus rapidly, suggesting either limited variation within populations or costs of increased tolerance. To measure possible costs of thermal tolerance, we selected for increased upper lethal limits for 10 generations in 22 lines of T. californicus from six populations. Then, for each line, we measured six fitness-related traits. Selected lines showed an overall increase in male and female body sizes, fecundity, and starvation resistance, suggesting a small benefit from (rather than costs of) increased tolerance. The effect of selection on correlated traits also varied significantly by population for five traits, indicating that the genetic basis for the selection response differed among populations. Our results suggest that adaptation was limited by the presence of variation within isolated populations rather than by costs of increased tolerance.

Summary Ocean acidification, caused by the uptake of atmospheric CO2, is a threat to marine biodiversity, potentially rivalling the threat imposed by rising temperatures in some marine ecosystems. Although a growing body of literature documents negative effects of acidification on marine organisms, the majority of this work has focused on the effects of future conditions on modern populations, ignoring the potential effects of adaptation and physiological acclimatization. We review current literature on the potential for adaptation to elevated pCO2 in marine organisms. Although this body of work is currently quite small, we argue that data on the physiological effects of acidification, natural variation in pH and lessons learned from previous work on thermal adaptation can all inform predictions and priorities for future research. Spatially varying selection is one of the most important forces maintaining intraspecific genetic variation. Unlike temperature, pH lacks a strong and persistent global gradient, and so selection may maintain less adaptive variation for pH than for temperature. On the other hand, we are only beginning to amass long-term data sets for pH variation in natural habitats, and thus, pH gradients may be more common than previously observed. Two of the most important effects of elevated pCO2 are reduced calcification and changes in metabolism. We discuss the ways that a detailed understanding of the physiological mechanisms underlying these effects is key to predicting the capacity for acclimatization and adaptation. Important priorities for future research will be to assess local adaptation to pH conditions and to measure the capacity for adaptation to future acidified conditions in natural populations. Tools for this work include traditional quantitative genetics, transcriptomics and the adaptation of ion-sensitive field-effect transistor (ISFET) technology for use in continuous seawater pH monitoring in the field.

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO 2 , will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins ( Strongylocentrotus purpuratus ) from the northeast Pacific Ocean. In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (13°C and 18°C) and pCO 2 (400 and 1100 μatm) conditions. Simultaneous exposure to increased temperature and pCO 2 significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO 2 but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species.

A rapidly growing body of literature documents the potential negative effects of CO2 -driven ocean acidification (OA) on marine organisms. However, nearly all this work has focused on the effects of future conditions on modern populations, neglecting the role of adaptation. Rapid evolution can alter demographic responses to environmental change, ultimately affecting the likelihood of population persistence, but the capacity for adaptation will differ among populations and species. Here, we measure the capacity of the ecologically important purple sea urchin Strongylocentrotus purpuratus to adapt to OA, using a breeding experiment to estimate additive genetic variance for larval size (an important component of fitness) under future high-pCO2 /low-pH conditions. Although larvae reared under future conditions were smaller than those reared under present-day conditions, we show that there is also abundant genetic variation for body size under elevated pCO2 , indicating that this trait can evolve. The observed heritability of size was 0.40 ± 0.32 (95% CI) under low pCO2 , and 0.50 ± 0.30 under high-pCO2 conditions. Accounting for the observed genetic variation in models of future larval size and demographic rates substantially alters projections of performance for this species in the future ocean. Importantly, our model shows that after incorporating the effects of adaptation, the OA-driven decrease in population growth rate is up to 50% smaller, than that predicted by the 'no-adaptation' scenario. Adults used in the experiment were collected from two sites on the coast of the Northeast Pacific that are characterized by different pH regimes, as measured by autonomous sensors. Comparing results between sites, we also found subtle differences in larval size under high-pCO2 rearing conditions, consistent with local adaptation to carbonate chemistry in the field. These results suggest that spatially varying selection may help to maintain genetic variation necessary for adaptation to future OA.

The extent to which acclimation and genetic adaptation might buffer natural populations against climate change is largely unknown. Most models predicting biological responses to environmental change assume that species' climatic envelopes are homogeneous both in space and time. Although recent discussions have questioned this assumption, few empirical studies have characterized intraspecific patterns of genetic variation in traits directly related to environmental tolerance limits. We test the extent of such variation in the broadly distributed tidepool copepod Tigriopus californicus using laboratory rearing and selection experiments to quantify thermal tolerance and scope for adaptation in eight populations spanning more than 17° of latitude. Tigriopus californicus exhibit striking local adaptation to temperature, with less than 1 per cent of the total quantitative variance for thermal tolerance partitioned within populations. Moreover, heat-tolerant phenotypes observed in low-latitude populations cannot be achieved in high-latitude populations, either through acclimation or 10 generations of strong selection. Finally, in four populations there was no increase in thermal tolerance between generations 5 and 10 of selection, suggesting that standing variation had already been depleted. Thus, plasticity and adaptation appear to have limited capacity to buffer these isolated populations against further increases in temperature. Our results suggest that models assuming a uniform climatic envelope may greatly underestimate extinction risk in species with strong local adaptation.

Species distribution modeling is the most common method of estimating climate change impacts on biodiversity. In this review, we argue a need for collaboration among physiologists, modelers and conservationists to parameterize models with physiological information in order to increase their accuracy and advance the field of conservation physiology., Climate change conservation planning relies heavily on correlative species distribution models that estimate future areas of occupancy based on environmental conditions encountered in present-day ranges. The approach benefits from rapid assessment of vulnerability over a large number of organisms, but can have poor predictive power when transposed to novel environments and reveals little in the way of causal mechanisms that define changes in species distribution or abundance. Having conservation planning rely largely on this single approach also increases the risk of policy failure. Mechanistic models that are parameterized with physiological information are expected to be more robust when extrapolating distributions to future environmental conditions and can identify physiological processes that set range boundaries. Implementation of mechanistic species distribution models requires knowledge of how environmental change influences physiological performance, and because this information is currently restricted to a comparatively small number of well-studied organisms, use of mechanistic modelling in the context of climate change conservation is limited. In this review, we propose that the need to develop mechanistic models that incorporate physiological data presents an opportunity for physiologists to contribute more directly to climate change conservation and advance the field of conservation physiology. We begin by describing the prevalence of species distribution modelling in climate change conservation, highlighting the benefits and drawbacks of both mechanistic and correlative approaches. Next, we emphasize the need to expand mechanistic models and discuss potential metrics of physiological performance suitable for integration into mechanistic models. We conclude by summarizing other factors, such as the need to consider demography, limiting broader application of mechanistic models in climate change conservation. Ideally, modellers, physiologists and conservation practitioners would work collaboratively to build models, interpret results and consider conservation management options, and articulating this need here may help to stimulate collaboration.