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Tooth classes are an innovation that has contributed to the evolutionary success of mammals. However, our understanding of the mechanisms by which tooth classes diversified remain limited. We use the evolutionary radiation of noctilionoid bats to show how the tooth developmental program evolved during the adaptation to new diet types. Combining morphological, developmental and mathematical modeling approaches, we demonstrate that tooth classes develop through independent developmental cascades that deviate from classical models. We show that the diversification of tooth number and size is driven by jaw growth rate modulation, explaining the rapid gain/loss of teeth in this clade. Finally, we mathematically model the successive appearance of tooth buds, supporting the hypothesis that growth acts as a key driver of the evolution of tooth number and size. Our work reveal how growth, by tinkering with reaction/diffusion processes, drives the diversification of tooth classes and other repeated structure during adaptive radiations.

Climate change drives species distribution shifts, affecting the availability of resources people rely upon for food and livelihoods. These impacts are complex, manifest at local scales, and have diverse effects across multiple species. However, for wild capture fisheries, current understanding is dominated by predictions for individual species at coarse spatial scales. We show that species-specific responses to localized environmental changes will alter the collection of co-occurring species within established fishing footprints along the U.S. West Coast. We demonstrate that availability of the most economically valuable, primary target species is highly likely to decline coastwide in response to warming and reduced oxygen concentrations, while availability of the most abundant, secondary target species will potentially increase. A spatial reshuffling of primary and secondary target species suggests regionally heterogeneous opportunities for fishers to adapt by changing where or what they fish. Developing foresight into the collective responses of species at local scales will enable more effective and tangible adaptation pathways for fishing communities.

Damselflies and dragonflies (Order: Odonata) play important roles in both aquatic and terrestrial food webs and can serve as sentinels of ecosystem health and predictors of population trends in other taxa. The habitat requirements and limited dispersal of lotic damselflies make them especially sensitive to habitat loss and fragmentation. As such, landscape genomic studies of these taxa can help focus conservation efforts on watersheds with high levels of genetic diversity, local adaptation, and even cryptic endemism. Here, as part of the California Conservation Genomics Project (CCGP), we report the first reference genome for the American rubyspot damselfly, Hetaerina americana, a species associated with springs, streams and rivers throughout California. Following the CCGP assembly pipeline, we produced two de novo genome assemblies. The primary assembly includes 1,630,044,487 base pairs, with a contig N50 of 5.4 Mb, a scaffold N50 of 86.2 Mb, and a BUSCO completeness score of 97.6%. This is the seventh Odonata genome to be made publicly available and the first for the subfamily Hetaerininae. This reference genome fills an important phylogenetic gap in our understanding of Odonata genome evolution, and provides a genomic resource for a host of interesting ecological, evolutionary, and conservation questions for which the rubyspot damselfly genus Hetaerina is an important model system.

Physical activity is associated with beneficial adaptations in human and rodent metabolism. We studied over 50 complex traits before and after exercise intervention in middle-aged men and a panel of 100 diverse strains of female mice. Candidate gene analyses in three brain regions, muscle, liver, heart, and adipose tissue of mice indicate genetic drivers of clinically relevant traits, including volitional exercise volume, muscle metabolism, adiposity, and hepatic lipids. Although ∼33% of genes differentially expressed in skeletal muscle following the exercise intervention are similar in mice and humans independent of BMI, responsiveness of adipose tissue to exercise-stimulated weight loss appears controlled by species and underlying genotype. We leveraged genetic diversity to generate prediction models of metabolic trait responsiveness to volitional activity offering a framework for advancing personalized exercise prescription. The human and mouse data are publicly available via a user-friendly Web-based application to enhance data mining and hypothesis development.

Phenotypic convergence across distantly related taxa can be driven by similar selective pressures from the environment or intrinsic constraints. The roles of these processes on physiological strategies, such as homeothermy, are poorly understood. We studied the evolution of thermal properties of mammalian pelage in a diverse community of rodents inhabiting the Mojave Desert, USA. We used a heat flux device to measure the thermal insulation of museum specimens and determined whether thermal properties were associated with habitat preferences while assessing phylogenetic dependence. Species that prefer arid habitats exhibited lower conductivity and thinner pelage relative to species with other habitat preferences. Despite being thinner, the pelage of arid species exhibited comparable insulation to the pelage of the other species due to its lower conductivity. Thus, arid species have insulative pelage while simultaneously benefitting from thin pelage that promotes convective cooling. We found no evidence of intrinsic constraints or phylogenetic dependence, indicating pelage readily evolves to environmental pressures. Thermoregulatory simulations demonstrated that arid specialists reduced energetic costs required for homeothermy by 14.5% by evolving lower conductivity, providing support for adaptive evolution of pelage. Our study indicates that selection for lower energetic requirements of homeothermy has shaped evolution of pelage thermal properties.

Notothenioidei fishes have evolved under stable cold temperatures; however, ocean conditions are changing globally, with polar regions poised to experience the greatest changes in environmental factors, such as warming. These stressors have the potential to dramatically affect energetic demands, and the persistence of the notothenioids will be dependent on metabolic capacity, or the ability to match energy supply with energy demand, to restore homeostasis in the face of changing climate conditions. In this study we examined aerobic metabolic capacity in three species, Trematomus bernacchii, T. pennellii and T. newnesi, and between two life stages, juvenile and adult, by assessing mitochondrial function of permeabilized cardiac fibers. Respiratory capacity differed among the adult notothenioids in this study, with greater oxidative phosphorylation (OXPHOS) respiration in the pelagic T. newnesi than the benthic T. bernacchii and T. pennellii. The variation in mitochondrial respiratory capacity was likely driven by differences in the mitochondrial content, as measured by citrate synthase activity, which was the highest in T. newnesi. In addition to high OXPHOS, T. newnesi exhibited lower LEAK respiration, resulting in greater mitochondrial efficiency than either T. bernacchii or T. pennellii. Life stage largely had an effect on mitochondrial efficiency and excess complex IV capacity, but there were little differences in OXPHOS respiration and electron transfer capacity, pointing to a lack of significant differences in the metabolic capacity between juveniles and adults. Overall, these results demonstrate species-specific differences in cardiac metabolic capacity, which may influence the acclimation potential of notothenioid fishes to changing environmental conditions.

In the last 300 thousand years, the genus Chlorocebus expanded from equatorial Africa into the southernmost latitudes of the continent, where colder climate was a probable driver of natural selection. We investigated population-level genetic variation in the mitochondrial uncoupling protein 1 (UCP1) gene region-implicated in non-shivering thermogenesis (NST)-in 73 wild savannah monkeys from three taxa representing this southern expansion (Chlorocebus pygerythrus hilgerti, Chlorocebus cynosuros and Chlorocebus pygerythrus pygerythrus) ranging from Kenya to South Africa. We found 17 single nucleotide polymorphisms with extended haplotype homozygosity consistent with positive selective sweeps, 10 of which show no significant linkage disequilibrium with each other. Phylogenetic generalized least-squares modelling with ecological covariates suggest that most derived allele frequencies are significantly associated with solar irradiance and winter precipitation, rather than overall low temperatures. This selection and association with irradiance is demonstrated by a relatively isolated population in the southern coastal belt of South Africa. We suggest that sunbathing behaviours common to savannah monkeys, in combination with the strength of solar irradiance, may mediate adaptations to thermal stress via NST among savannah monkeys. The variants we discovered all lie in non-coding regions, some with previously documented regulatory functions, calling for further validation and research.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Direct observation of evolution in response to natural environmental change can resolve fundamental questions about adaptation, including its pace, temporal dynamics, and underlying phenotypic and genomic architecture. We tracked the evolution of fitness-associated phenotypes and allele frequencies genome-wide in 10 replicate field populations of Drosophila melanogaster over 10 generations from summer to late fall. Adaptation was evident over each sampling interval (one to four generations), with exceptionally rapid phenotypic adaptation and large allele frequency shifts at many independent loci. The direction and basis of the adaptive response shifted repeatedly over time, consistent with the action of strong and rapidly fluctuating selection. Overall, we found clear phenotypic and genomic evidence of adaptive tracking occurring contemporaneously with environmental change, thus demonstrating the temporally dynamic nature of adaptation.

Highly pleiotropic genes are predicted to be used less often during adaptation, as mutations in these loci are more likely to have negative fitness consequences. Following this logic, we tested whether pleiotropy impacts the probability that a locus will be used repeatedly in adaptation. We used two proxies to estimate pleiotropy: number of phenotypic traits affected by a given genomic region and gene connectivity. We first surveyed 16 independent stream-lake and three independent benthic-limnetic ecotype pairs of threespine stickleback to estimate genome-wide patterns in parallel genomic differentiation. Our analysis revealed parallel divergence across the genome; 30%-37% of outlier regions were shared between at least two independent pairs in either the stream-lake or benthic-limnetic comparisons. We then tested whether parallel genomic regions are less pleiotropic than nonparallel regions. Counter to our a priori prediction, parallel genomic regions contained genes with significantly more pleiotropy; that is, influencing a greater number of traits and more highly connected. The increased pleiotropy of parallel regions could not be explained by other genomic factors, as there was no significant difference in mean gene count, mutation or recombination rates between parallel and nonparallel regions. Interestingly, although nonparallel regions contained genes that were less connected and influenced fewer mapped traits on average than parallel regions, they also tended to contain the genes that were predicted to be the most pleiotropic. Taken together, our findings are consistent with the idea that pleiotropy only becomes constraining at high levels and that low or intermediate levels of pleiotropy may be beneficial for adaptation.

The first Editor of Evolution was Ernst Mayr. His foreword to the first issue of Evolution published in 1947 framed evolution as a "problem of interaction" that was just beginning to be studied in this broad context. First, I explore progress and prospects on understanding the subsidiary interactions identified by Mayr, including interactions between parts of organisms, between individuals and populations, between species, and between the organism and its abiotic environment. Mayr's overall "problem of interaction" framework is examined in the context of coevolution within and among levels of biological organization. This leads to a comparison in the relative roles of biotic versus abiotic agents of selection and fluctuating versus directional selection, followed by stabilizing selection in shaping the genomic architecture of adaptation. Oligogenic architectures may be typical for traits shaped more by fluctuating selection and biotic selection. Conversely, polygenic architectures may be typical for traits shaped more by directional followed by stabilizing selection and abiotic selection. The distribution of effect sizes and turnover dynamics of adaptive alleles in these scenarios deserves further study. Second, I review two case studies on the evolution of acquired toxicity in animals, one involving cardiac glycosides obtained from plants and one involving bacterial virulence factors horizontally transferred to animals. The approaches used in these studies and the results gained directly flow from Mayr's vision of an evolutionary biology that revolves around the "problem of interaction."

White seabass (Atractoscion nobilis) increasingly experience periods of low oxygen (O2; hypoxia) and high carbon dioxide (CO2, hypercapnia) due to climate change and eutrophication of the coastal waters of California. Hemoglobin (Hb) is the principal O2 carrier in the blood and in many teleost fishes Hb-O2 binding is compromised at low pH; however, the red blood cells (RBC) of some species regulate intracellular pH with adrenergically stimulated sodium-proton-exchangers (β-NHEs). We hypothesized that RBC β-NHEs in white seabass are an important mechanism that can protect the blood O2-carrying capacity during hypoxia and hypercapnia. We determined the O2-binding characteristics of white seabass blood, the cellular and subcellular response of RBCs to adrenergic stimulation, and quantified the protective effect of β-NHE activity on Hb-O2 saturation. White seabass had typical teleost Hb characteristics, with a moderate O2 affinity (Po2 at half-saturation; P50 2.9 kPa) that was highly pH-sensitive (Bohr coefficient -0.92; Root effect 52%). Novel findings from super-resolution microscopy revealed β-NHE protein in vesicle-like structures and its translocation into the membrane after adrenergic stimulation. Microscopy data were corroborated by molecular and phylogenetic results and a functional characterization of β-NHE activity. The activation of RBC β-NHEs increased Hb-O2 saturation by ∼8% in normoxic hypercapnia and by up to ∼20% in hypoxic normocapnia. Our results provide novel insight into the cellular mechanism of adrenergic RBC stimulation within an ecologically relevant context. β-NHE activity in white seabass has great potential to protect arterial O2 transport during hypoxia and hypercapnia but is less effective during combinations of these stressors.

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

Deserts are among the harshest environments on Earth. The multiple ages of different deserts and their global distribution provide a unique opportunity to study repeated adaptation at different timescales. Here, we summarize recent genomic research on the genetic mechanisms underlying desert adaptations in mammals. Several studies on different desert mammals show large overlap in functional classes of genes and pathways, consistent with the complexity and variety of phenotypes associated with desert adaptation to water and food scarcity and extreme temperatures. However, studies of desert adaptation are also challenged by a lack of accurate genotype-phenotype-environment maps. We encourage development of systems that facilitate functional analyses, but also acknowledge the need for more studies on a wider variety of desert mammals.

Thermal adaptation to habitat variability can determine species vulnerability to environmental change. For example, physiological tolerance to naturally low thermal variation in tropical forests species may alter their vulnerability to climate change impacts, compared with open habitat species. However, the extent to which habitat-specific differences in tolerance derive from within-generation versus across-generation ecological or evolutionary processes are not well characterized. Here we studied thermal tolerance limits of a Central African butterfly (Bicyclus dorothea) across two habitats in Cameroon: a thermally stable tropical forest and the more variable ecotone between rainforest and savanna. Second generation individuals originating from the ecotone, reared under conditions common to both populations, exhibited higher upper thermal limits (CTmax) than individuals originating from forest (∼3°C greater). Lower thermal limits (CTmin) were also slightly lower for the ecotone populations (∼1°C). Our results are suggestive of local adaptation driving habitat-specific differences in thermal tolerance (especially CTmax) that hold across generations. Such habitat-specific thermal limits may be widespread for tropical ectotherms and could affect species vulnerability to environmental change. However, microclimate and within-generation developmental processes (e.g. plasticity) will mediate these differences, and determining the fitness consequences of thermal variation for ecotone and rainforest species will require continued study of both within-generation and across-generation eco-evolutionary processes.This article has an associated First Person interview with the first author of the paper.

Temporal genomic data hold great potential for studying evolutionary processes such as speciation. However, sampling across speciation events would, in many cases, require genomic time series that stretch well back into the Early Pleistocene subepoch. Although theoretical models suggest that DNA should survive on this timescale1, the oldest genomic data recovered so far are from a horse specimen dated to 780-560 thousand years ago2. Here we report the recovery of genome-wide data from three mammoth specimens dating to the Early and Middle Pleistocene subepochs, two of which are more than one million years old. We find that two distinct mammoth lineages were present in eastern Siberia during the Early Pleistocene. One of these lineages gave rise to the woolly mammoth and the other represents a previously unrecognized lineage that was ancestral to the first mammoths to colonize North America. Our analyses reveal that the Columbian mammoth of North America traces its ancestry to a Middle Pleistocene hybridization between these two lineages, with roughly equal admixture proportions. Finally, we show that the majority of protein-coding changes associated with cold adaptation in woolly mammoths were already present one million years ago. These findings highlight the potential of deep-time palaeogenomics to expand our understanding of speciation and long-term adaptive evolution.

While it has been hypothesized that brown adipocytes responsible for mammalian thermogenesis are absent in birds, the existence of beige fat has yet to be studied directly. The present study tests the hypothesis that beige fat emerges in birds as a mechanism of physiological adaptation to cold environments. Subcutaneous neck adipose tissue from cold-acclimated or triiodothyronine (T3)-treated chickens exhibited increases in the expression of avian uncoupling protein (avUCP, an ortholog of mammalian UCP2 and UCP3) gene and some known mammalian beige adipocyte-specific markers. Morphological characteristics of white adipose tissues of treated chickens showed increased numbers of both small and larger clusters of multilocular fat cells within the tissues. Increases in protein levels of avUCP and mitochondrial marker protein, voltage-dependent anion channel, and immunohistochemical analysis for subcutaneous neck fat revealed the presence of potentially thermogenic mitochondria-rich cells. This is the first evidence that the capacity for thermogenesis may be acquired by differentiating adipose tissue into beige-like fat for maintaining temperature homeostasis in the subcutaneous fat 'neck warmer' in chickens exposed to a cold environment.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

This study uncovers a correlation between the mid-infrared emissivity of butterfly wings and the average air temperature of their habitats across the world. Butterflies from cooler climates have a lower mid-infrared emissivity, which limits heat losses to surroundings, and butterflies from warmer climates have a higher mid-infrared emissivity, which enhances radiative cooling. The mid-infrared emissivity showed no correlation with other investigated climatic factors. Phylogenetic independent contrasts analysis indicates the microstructures of butterfly wings may have evolved in part to regulate mid-infrared emissivity as an adaptation to climate, rather than as phylogenetic inertia. Our findings offer new insights into the role of microstructures in thermoregulation and suggest both evolutionary and physical constraints to butterflies' abilities to adapt to climate change.

Advances in genomics have expedited the improvement of several agriculturally important crops but similar efforts in wheat (Triticum spp.) have been more challenging. This is largely owing to the size and complexity of the wheat genome1, and the lack of genome-assembly data for multiple wheat lines2,3. Here we generated ten chromosome pseudomolecule and five scaffold assemblies of hexaploid wheat to explore the genomic diversity among wheat lines from global breeding programs. Comparative analysis revealed extensive structural rearrangements, introgressions from wild relatives and differences in gene content resulting from complex breeding histories aimed at improving adaptation to diverse environments, grain yield and quality, and resistance to stresses4,5. We provide examples outlining the utility of these genomes, including a detailed multi-genome-derived nucleotide-binding leucine-rich repeat protein repertoire involved in disease resistance and the characterization of Sm16, a gene associated with insect resistance. These genome assemblies will provide a basis for functional gene discovery and breeding to deliver the next generation of modern wheat cultivars.

Rapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data (e.g., evolve-and-resequence studies). These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one time point to be predictive of the changes at later time points, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time points and across replicates. We estimate that at least 17 to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances, we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.

In temperate climates, the recurring seasonal exigencies of winter represent a fundamental physiological challenge for a wide range of organisms. In response, many temperate insects enter diapause, an alternative developmental program, including developmental arrest, that allows organisms to synchronize their life cycle with seasonal environmental variation. Geographic variation in diapause phenology contributing to local climatic adaptation is well documented. However, few studies have examined how the rapid evolution of a suite of traits expressed across the diapause program may contribute to climatic adaptation on a contemporary timescale. Here, we investigate the evolution of the diapause program over the past 35 years by leveraging a natural experiment presented by the recent invasion of the Asian tiger mosquito, Aedes albopictus, across the eastern United States. We sampled populations from two distinct climatic regions separated by 6° of latitude (∼700 km). Using common-garden experiments, we identified regional genetic divergence in diapause-associated cold tolerance, diapause duration, and postdiapause starvation tolerance. We also found regional divergence in nondiapause thermal performance. In contrast, we observed minimal regional divergence in nondiapause larval growth traits and at neutral molecular marker loci. Our results demonstrate rapid evolution of the diapause program and imply strong selection caused by differences in winter conditions.

The cave bear is one of the best known extinct large mammals that inhabited Europe during the "Ice Age," becoming extinct ≈24,000 years ago along with other members of the Pleistocene megafauna. Long-standing hypotheses speculate that many cave bears died during their long hibernation periods, which were necessary to overcome the severe and prolonged winters of the Last Glacial. Here, we investigate how long hibernation periods in cave bears would have directly affected their feeding biomechanics using CT-based biomechanical simulations of skulls of cave and extant bears. Our results demonstrate that although large paranasal sinuses were necessary for, and consistent with, long hibernation periods, trade-offs in sinus-associated cranial biomechanical traits restricted cave bears to feed exclusively on low energetic vegetal resources during the predormancy period. This biomechanical trade-off constitutes a new key factor to mechanistically explain the demise of this dominant Pleistocene megafaunal species as a direct consequence of climate cooling.

Temperature is known to influence many aspects of organisms and is frequently linked to geographical species distributions. Despite the importance of a broad understanding of an animal's thermal biology, few studies incorporate more than one metric of thermal biology. Here we examined an elevational assemblage of Habronattus jumping spiders to measure different aspects of their thermal biology including thermal limits (CTmin, CTmax), thermal preference, V̇CO2 as proxy for metabolic rate, locomotor behavior and warming tolerance. We used these data to test whether thermal biology helped explain how species were distributed across elevation. Habronattus had high CTmax values, which did not differ among species across the elevational gradient. The highest-elevation species had a lower CTmin than any other species. All species had a strong thermal preference around 37 °C. With respect to performance, one of the middle elevation species was significantly less temperature-sensitive in metabolic rate. Differences between species with respect to locomotion (jump distance) were likely driven by differences in mass, with no differences in thermal performance across elevation. We suggest that Habronattus distributions follow Brett's rule, a rule that predicts more geographical variation in cold tolerance than heat. Additionally, we suggest that physiological tolerances interact with biotic factors, particularly those related to courtship and mate choice to influence species distributions. Habronattus also had very high warming tolerance values (> 20 °C, on average). Taken together, these data suggest that Habronattus are resilient in the face of climate-change related shifts in temperature.

Helping the world's coastal communities adapt to climate change impacts requires evaluating the vulnerability of coastal communities and assessing adaptation options. This includes understanding the potential for 'natural' infrastructure (ecosystems and the biodiversity that underpins them) to reduce communities' vulnerability, alongside more traditional 'hard' infrastructure approaches. Here we present a spatially explicit global evaluation of the vulnerability of coastal-dwelling human populations to key climate change exposures and explore the potential for coastal ecosystems to help people adapt to climate change (ecosystem-based adaptation (EbA)). We find that mangroves and coral reefs are particularly well situated to help people cope with current weather extremes, a function that will only increase in importance as people adapt to climate change now and in coming decades. We find that around 30.9 million people living within 2km of the coast are highly vulnerable to tropical storms and sea-level rise (SLR). Mangroves and coral reefs overlap these threats to at least 5.3 and 3.4 million people, respectively, with substantial potential to dissipate storm surges and improve resilience against SLR effects. Significant co-benefits from mangroves also accrue, with 896 million metric tons of carbon stored in their soils and above- and below-ground biomass. Our framework offers a tool for prioritizing 'hotspots' of coastal EbA potential for further, national and local analyses to quantify risk reduction and, thereby, guide investment in coastal ecosystems to help people adapt to climate change. In doing so, it underscores the global role that conserving and restoring ecosystems can play in protecting human lives and livelihoods, as well as biodiversity, in the face of climate change.

Climate change-induced extinctions are estimated to eliminate one in six known species by the end of the century. One major factor that will contribute to these extinctions is extreme climatic events. Here, we show the ecological impacts of recent record warm air temperatures and simultaneous peak drought conditions in California. From 2008-2016, the southern populations of a wide-ranging endemic amphibian (the California newt, Taricha torosa) showed a 20% reduction to mean body condition and significant losses to variation in body condition linked with extreme climate deviations. However, body condition in northern populations remained relatively unaffected during this period. Range-wide population estimates of change to body condition under future climate change scenarios within the next 50 years suggest that northern populations will mirror the loss of body condition recently observed in southern populations. This change is predicated on latter 21st century climate deviations that resemble recent conditions in Southern California. Thus, the ecological consequences of climate change have already occurred across the warmer, drier regions of Southern California, and our results suggest that predicted climate vulnerable regions in the more mesic northern range likely will not provide climate refuge for numerous amphibian communities.

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from the repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we use three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification.

In response to environmental change, organisms rely on both genetic adaptation and phenotypic plasticity to adjust key traits that are necessary for survival and reproduction. Given the accelerating rate of climate change, plasticity may be particularly important. For organisms in warming aquatic habitats, upper thermal tolerance is likely to be a key trait, and many organisms express plasticity in this trait in response to developmental or adulthood temperatures. Although plasticity at one life stage may influence plasticity at another life stage, relatively little is known about this possibility for thermal tolerance. Here, we used locally adapted populations of the copepod Tigriopus californicus to investigate these potential effects in an intertidal ectotherm. We found that low latitude populations had greater critical thermal maxima (CTmax) than high latitude populations, and variation in developmental temperature altered CTmax plasticity in adults. After development at 25°C, CTmax was plastic in adults, whereas no adulthood plasticity in this trait was observed after development at 20°C. This pattern was identical across four populations, suggesting that local thermal adaptation has not shaped this effect among these populations. Differences in the capacities to maintain ATP synthesis rates and to induce heat shock proteins at high temperatures, two likely mechanisms of local adaptation in this species, were consistent with changes in CTmax owing to phenotypic plasticity, which suggests that there is likely mechanistic overlap between the effects of plasticity and adaptation. Together, these results indicate that developmental effects may have substantial impacts on upper thermal tolerance plasticity in adult ectotherms.

The current trajectory for crop yields is insufficient to nourish the world's population by 20501. Greater and more consistent crop production must be achieved against a backdrop of climatic stress that limits yields, owing to shifts in pests and pathogens, precipitation, heat-waves and other weather extremes. Here we consider the potential of plant sciences to address post-Green Revolution challenges in agriculture and explore emerging strategies for enhancing sustainable crop production and resilience in a changing climate. Accelerated crop improvement must leverage naturally evolved traits and transformative engineering driven by mechanistic understanding, to yield the resilient production systems that are needed to ensure future harvests.

Ocean acidification is expected to negatively impact calcifying organisms, yet we lack understanding of their acclimation potential in the natural environment. Here we measured geochemical proxies (δ11B and B/Ca) in Porites astreoides corals that have been growing for their entire life under low aragonite saturation (Ωsw: 0.77-1.85). This allowed us to assess the ability of these corals to manipulate the chemical conditions at the site of calcification (Ωcf), and hence their potential to acclimate to changing Ωsw. We show that lifelong exposure to low Ωsw did not enable the corals to acclimate and reach similar Ωcf as corals grown under ambient conditions. The lower Ωcf at the site of calcification can explain a large proportion of the decreasing P. astreoides calcification rates at low Ωsw. The naturally elevated seawater dissolved inorganic carbon concentration at this study site shed light on how different carbonate chemistry parameters affect calcification conditions in corals.

Monitor lizards are unique among ectothermic reptiles in that they have high aerobic capacity and distinctive cardiovascular physiology resembling that of endothermic mammals. Here, we sequence the genome of the Komodo dragon Varanus komodoensis, the largest extant monitor lizard, and generate a high-resolution de novo chromosome-assigned genome assembly for V. komodoensis using a hybrid approach of long-range sequencing and single-molecule optical mapping. Comparing the genome of V. komodoensis with those of related species, we find evidence of positive selection in pathways related to energy metabolism, cardiovascular homoeostasis, and haemostasis. We also show species-specific expansions of a chemoreceptor gene family related to pheromone and kairomone sensing in V. komodoensis and other lizard lineages. Together, these evolutionary signatures of adaptation reveal the genetic underpinnings of the unique Komodo dragon sensory and cardiovascular systems, and suggest that selective pressure altered haemostasis genes to help Komodo dragons evade the anticoagulant effects of their own saliva. The Komodo dragon genome is an important resource for understanding the biology of monitor lizards and reptiles worldwide.

California mice (Peromyscus californicus) differ from most other mammals in that they are biparental, genetically monogamous, and (compared with other Peromyscus) relatively large. We evaluated effects of cold acclimation on metabolic rate, exercise performance, and morphology of pair-housed male California mice, as well as modulation of these effects by fatherhood. In Experiment 1, virgin males housed at 5° or 10 °C for approximately 25 days were compared with virgins housed at standard vivarium temperature of 22 °C. Measures included resting metabolic rate (RMR), maximal oxygen consumption ([Formula: see text]max), grip strength, and sprint speed. In Experiment 2, virgin males housed at 22 °C were compared with three groups of males housed at 10 °C: virgins, breeding males (housed with a female and their pups), and non-breeding males (housed with an ovariectomized, estrogen- and progesterone-treated female) after long-term acclimation (mean 243 days). Measures in this experiment included basal metabolic rate (BMR), [Formula: see text]max, maximal thermogenic capacity ([Formula: see text]sum), and morphological traits. In Experiment 1, virgin males housed at 5° and 10 °C had higher RMR and [Formula: see text]max than those at 22 °C. In Experiment 2, 10 °C-acclimated groups had shorter bodies; increased body, fat, and lean masses; higher BMR and [Formula: see text]sum, and generally greater morphometric measures and organ masses than virgin males at 22 °C. Among the groups housed at 10 °C, breeding males had higher BMR and lower [Formula: see text]max than non-breeding and/or virgin males. Overall, we found that effects of fatherhood during cold acclimation were inconsistent, and that several aspects of cold acclimation differ substantially between California mice and other small mammals.

Coral calcification is expected to decline as atmospheric carbon dioxide concentration increases. We assessed the potential of Porites astreoides, Siderastrea siderea and Porites porites to survive and calcify under acidified conditions in a 2-year field transplant experiment around low pH, low aragonite saturation (Ωarag) submarine springs. Slow-growing S. siderea had the highest post-transplantation survival and showed increases in concentrations of Symbiodiniaceae, chlorophyll a and protein at the low Ωarag site. Nubbins of P. astreoides had 20% lower survival and higher chlorophyll a concentration at the low Ωarag site. Only 33% of P. porites nubbins survived at low Ωarag and their linear extension and calcification rates were reduced. The density of skeletons deposited after transplantation at the low Ωarag spring was 15-30% lower for all species. These results suggest that corals with slow calcification rates and high Symbiodiniaceae, chlorophyll a and protein concentrations may be less susceptible to ocean acidification, albeit with reduced skeletal density. We postulate that corals in the springs are responding to greater energy demands for overcoming larger differences in carbonate chemistry between the calcifying medium and the external environment. The differential mortality, growth rates and physiological changes may impact future coral species assemblages and the reef framework robustness.

The transient receptor potential vanilloid 1 (TRPV1) ion channel is a prototypical molecular sensor for noxious heat in mammals. Its role in sustained heat response remains poorly understood, because rapid heat-induced desensitization (Dh) follows tightly heat-induced activation (Ah). To understand the physiological role and structural basis of Dh, we carried out a comparative study of TRPV1 channels in mouse (mV1) and those in platypus (pV1), which naturally lacks Dh. Here we show that a temperature-sensitive interaction between the N- and C-terminal domains of mV1 but not pV1 drives a conformational rearrangement in the pore leading to Dh. We further show that knock-in mice expressing pV1 sensed heat normally but suffered scald damages in a hot environment. Our findings suggest that Dh evolved late during evolution as a protective mechanism and a delicate balance between Ah and Dh is crucial for mammals to sense and respond to noxious heat.

Previous studies have demonstrated reduced performance in triploid fish when reared under suboptimal conditions, which may be the result of a higher susceptibility to stressors when compared to diploids. The goal of this project was to investigate differences in the capacity of diploid (8 N) and triploid (12 N) white sturgeon, Acipenser transmontanus, to respond to both warm acclimation (6-weeks of acclimation to either 18 or 22 °C) and a subsequent acute stress (10-min low water stress). Following the 6-week acclimation, fish were sampled either before or following an acute low water stress. Bioindices of the primary and secondary stress response, hematology and cellular metabolic status were measured. We also sought to determine if time to peak cortisol levels were similar between diploid and triploid sturgeon after exposure to a severe acute stressor (netting stress). While both ploidies had similar primary and secondary responses to acute stress, both with and without warm acclimation, warm acclimation impacted the ability of diploid and triploid white sturgeon to mount a typical stress response to an acute stressor. In response to warm acclimation, triploids exhibited little change in branchial lactate dehydrogenase activity, while diploids increased activity. After exposure to an acute water reduction stress, diploids increased citrate synthase activity, yet triploids showed a decrease in activity. Differences in metabolic enzyme activity in response to warm acclimation and acute stress suggest triploid white sturgeon may have a reduced cellular metabolic capacity under chronic and acute stress, which may impact performance of triploid sturgeon in suboptimal conditions.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

Environmental cues profoundly affect cellular plasticity in multicellular organisms. For instance, exercise promotes a glycolytic-to-oxidative fibre-type switch in skeletal muscle, and cold acclimation induces beige adipocyte biogenesis in adipose tissue. However, the molecular mechanisms by which physiological or pathological cues evoke developmental plasticity remain incompletely understood. Here we report a type of beige adipocyte that has a critical role in chronic cold adaptation in the absence of β-adrenergic receptor signalling. This beige fat is distinct from conventional beige fat with respect to developmental origin and regulation, and displays enhanced glucose oxidation. We therefore refer to it as glycolytic beige fat. Mechanistically, we identify GA-binding protein α as a regulator of glycolytic beige adipocyte differentiation through a myogenic intermediate. Our study reveals a non-canonical adaptive mechanism by which thermal stress induces progenitor cell plasticity and recruits a distinct form of thermogenic cell that is required for energy homeostasis and survival.

Previous studies suggest fish with additional copies of their genome (polyploids) underperform in suboptimal conditions and may be more susceptible to stress and disease. The objective of this study was to determine the role ploidy plays in the physiological response of white sturgeon to chronically elevated water temperatures. White sturgeon of two ploidies (8 N and 10 N) were acclimated to ambient (18 °C) and warm (22 °C) water. Bioindices of stress (plasma cortisol, glucose and lactate, total erythrocyte count, hematocrit, hemoglobin, mean erythrocyte volume, mean erythrocyte hemoglobin, and mean erythrocyte hemoglobin concentration), immunity (respiratory burst, plasma lysozyme, and total leukocyte count), and cellular metabolic capacity (lactate dehydrogenase and citrate synthase activity) were measured before and after a 6-week acclimation period. Both ploidies appear comparable in their constitutive immune and stress parameters and respond similarly to warming. Hematological indices suggest 8 N and 10 N sturgeon are similar in oxygen carrying capacity; however, differences in enzyme activity between ploidies indicate that 10 N sturgeon may have a lower cellular aerobic capacity. Our results have implications for the screening and management of ploidy on white sturgeon farms and hatcheries, as the differences between ploidies may affect 10 N sturgeon performance at elevated water temperatures. Further research is needed to elucidate the differences in inducible stress and immune responses and metabolism of white sturgeon of different ploidies.

Human-induced thermal variability can disrupt energy balance and performance in ectotherms; however, phenotypic plasticity may play a pivotal protective role. Ectotherm performance can be maintained in thermally heterogeneous habitats by reducing the thermal sensitivity of physiological processes and concomitant performance. We examined the capacity of juvenile green sturgeon (Acipenser medirostris) to respond to daily thermal variation. Juveniles (47 days post-hatch) were exposed to either stable (15 ± 0.5 °C) or variable (narrowly variable: 13-17 °C day-1 or widely variable 11-21 °C day-1) thermoperiod treatments, with equivalent mean temperatures (15 ± 0.5 °C), for 21 days. Growth (relative growth rate, % body mass gain), upper thermal tolerance (critical thermal maxima, CTMax) and the thermal sensitivity of swimming performance (critical swimming speed, Ucrit) were assessed in fish from all treatments. Accelerated growth was observed in fish maintained under widely variable temperatures compared to narrowly variable and stable temperatures. No significant variation in CTMax was observed among thermoperiod treatments, suggesting all treatment groups acclimated to the mean temperature rather than daily maximums. The widely variable treatment induced a plastic response in swimming performance, where Ucrit was insensitive to temperature and performance was maintained across a widened thermal breadth. Maximum Ucrit attained was similar among thermoperiod treatments, but performance was maximised at different test temperatures (stable: 4.62 ± 0.44 BL s-1 at 15 °C; narrowly variable: 4.52 ± 0.23 BL s-1 at 21 °C; widely variable: 3.90 ± 0.24 BL s-1 at 11 °C, mean ± s.e.m.). In combination, these findings suggest juvenile A. medirostris are resilient to daily fluctuations in temperature, within the temperature range tested here.

In insects and other ectotherms, cold temperatures cause a coma resulting from loss of neuromuscular function, during which ionic and metabolic homeostasis are progressively lost. Cold adaptation improves homeostasis during cold exposure, but the ultimate targets of selection are still an open question. Cold acclimation and adaptation remodels mitochondrial metabolism in insects, suggesting that aerobic energy production during cold exposure could be a target of selection. Here, we test the hypothesis that cold adaptation improves the ability to maintain rates of aerobic energy production during cold exposure by using 31 P NMR on live flies. Using lines of Drosophila melanogaster artificially selected for fast and slow recovery from a cold coma, we show that cold exposure does not lower ATP levels and that cold adaptation does not alter aerobic ATP production during cold exposure. Cold-hardy and cold-susceptible lines both experienced a brief transition to anaerobic metabolism during cooling, but this was rapidly reversed during cold exposure, suggesting that oxidative phosphorylation was sufficient to meet energy demands below the critical thermal minimum, even in cold-susceptible flies. We thus reject the hypothesis that performance under mild low temperatures is set by aerobic ATP supply limitations in D. melanogaster, excluding oxygen and capacity limitation as a weak link in energy supply. This work suggests that the modulations to mitochondrial metabolism resulting from cold acclimation or adaptation may arise from selection on a biosynthetic product(s) of those pathways rather than selection on ATP supply during cold exposure.

Adipocytes possess remarkable adaptive capacity to respond to nutrient excess, fasting or cold exposure, and they are thus an important cell type for the maintenance of proper metabolic health. Although the endoplasmic reticulum (ER) is a critical organelle for cellular homeostasis, the mechanisms that mediate adaptation of the ER to metabolic challenges in adipocytes are unclear. Here we show that brown adipose tissue (BAT) thermogenic function requires an adaptive increase in proteasomal activity to secure cellular protein quality control, and we identify the ER-localized transcription factor nuclear factor erythroid 2-like 1 (Nfe2l1, also known as Nrf1) as a critical driver of this process. We show that cold adaptation induces Nrf1 in BAT to increase proteasomal activity and that this is crucial for maintaining ER homeostasis and cellular integrity, specifically when the cells are in a state of high thermogenic activity. In mice, under thermogenic conditions, brown-adipocyte-specific deletion of Nfe2l1 (Nrf1) resulted in ER stress, tissue inflammation, markedly diminished mitochondrial function and whitening of the BAT. In mouse models of both genetic and dietary obesity, stimulation of proteasomal activity by exogenously expressing Nrf1 or by treatment with the proteasome activator PA28α in BAT resulted in improved insulin sensitivity. In conclusion, Nrf1 emerges as a novel guardian of brown adipocyte function, providing increased proteometabolic quality control for adapting to cold or to obesity.

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26 °C) and sub-bleaching (31 °C) temperatures under elevated nitrate. Warming to 31 °C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change.

Increases in atmospheric CO2 levels and associated ocean changes are expected to have dramatic impacts on marine ecosystems. Although the Southern Ocean is experiencing some of the fastest rates of change, few studies have explored how Antarctic fishes may be affected by co-occurring ocean changes, and even fewer have examined early life stages. To date, no studies have characterized potential trade-offs in physiology and behavior in response to projected multiple climate change stressors (ocean acidification and warming) on Antarctic fishes. We exposed juvenile emerald rockcod Trematomus bernacchii to three PCO2 treatments (~450, ~850, and ~1,200 μatm PCO2 ) at two temperatures (-1 or 2°C). After 2, 7, 14, and 28 days, metrics of physiological performance including cardiorespiratory function (heart rate [fH ] and ventilation rate [fV ]), metabolic rate (M˙O2), and cellular enzyme activity were measured. Behavioral responses, including scototaxis, activity, exploration, and escape response were assessed after 7 and 14 days. Elevated PCO2 independently had little impact on either physiology or behavior in juvenile rockcod, whereas warming resulted in significant changes across acclimation time. After 14 days, fH , fV and M˙O2 significantly increased with warming, but not with elevated PCO2 . Increased physiological costs were accompanied by behavioral alterations including increased dark zone preference up to 14%, reduced activity by 12%, as well as reduced escape time suggesting potential trade-offs in energetics. After 28 days, juvenile rockcod demonstrated a degree of temperature compensation as fV , M˙O2, and cellular metabolism significantly decreased following the peak at 14 days; however, temperature compensation was only evident in the absence of elevated PCO2 . Sustained increases in fV and M˙O2 after 28 days exposure to elevated PCO2 indicate additive (fV ) and synergistic (M˙O2) interactions occurred in combination with warming. Stressor-induced energetic trade-offs in physiology and behavior may be an important mechanism leading to vulnerability of Antarctic fishes to future ocean change.

Species respond to climate change in two dominant ways: range shifts in latitude or elevation and phenological shifts of life-history events. Range shifts are widely viewed as the principal mechanism for thermal niche tracking, and phenological shifts in birds and other consumers are widely understood as the principal mechanism for tracking temporal peaks in biotic resources. However, phenological and range shifts each present simultaneous opportunities for temperature and resource tracking, although the possible role for phenological shifts in thermal niche tracking has been widely overlooked. Using a canonical dataset of Californian bird surveys and a detectability-based approach for quantifying phenological signal, we show that Californian bird communities advanced their breeding phenology by 5-12 d over the last century. This phenological shift might track shifting resource peaks, but it also reduces average temperatures during nesting by over 1 °C, approximately the same magnitude that average temperatures have warmed over the same period. We further show that early-summer temperature anomalies are correlated with nest success in a continental-scale database of bird nests, suggesting avian thermal niches might be broadly limited by temperatures during nesting. These findings outline an adaptation surface where geographic range and breeding phenology respond jointly to constraints imposed by temperature and resource phenology. By stabilizing temperatures during nesting, phenological shifts might mitigate the need for range shifts. Global change ecology will benefit from further exploring phenological adjustment as a potential mechanism for thermal niche tracking and vice versa.

Human high-altitude (HA) adaptation or mal-adaptation is explored to understand the physiology, pathophysiology, and molecular mechanisms that underlie long-term exposure to hypoxia. Here, we report the results of an analysis of the largest whole-genome-sequencing of Chronic Mountain Sickness (CMS) and nonCMS individuals, identified candidate genes and functionally validated these candidates in a genetic model system (Drosophila). We used PreCIOSS algorithm that uses Haplotype Allele Frequency score to separate haplotypes carrying the favored allele from the noncarriers and accordingly, prioritize genes associated with the CMS or nonCMS phenotype. Haplotypes in eleven candidate regions, with SNPs mostly in nonexonic regions, were significantly different between CMS and nonCMS subjects. Closer examination of individual genes in these regions revealed the involvement of previously identified candidates (e.g., SENP1) and also unreported ones SGK3, COPS5, PRDM1, and IFT122 in CMS. Remarkably, in addition to genes like SENP1, SGK3, and COPS5 which are HIF-dependent, our study reveals for the first time HIF-independent gene PRDM1, indicating an involvement of wider, nonHIF pathways in HA adaptation. Finally, we observed that down-regulating orthologs of these genes in Drosophila significantly enhanced their hypoxia tolerance. Taken together, the PreCIOSS algorithm, applied on a large number of genomes, identifies the involvement of both new and previously reported genes in selection sweeps, highlighting the involvement of multiple hypoxia response systems. Since the overwhelming majority of SNPs are in nonexonic (and possibly regulatory) regions, we speculate that adaptation to HA necessitates greater genetic flexibility allowing for transcript variability in response to graded levels of hypoxia.

Geographically separated populations can convergently adapt to the same selection pressure. Convergent evolution at the level of a gene may arise via three distinct modes. The selected alleles can (1) have multiple independent mutational origins, (2) be shared due to shared ancestral standing variation, or (3) spread throughout subpopulations via gene flow. We present a model-based, statistical approach that utilizes genomic data to detect cases of convergent adaptation at the genetic level, identify the loci involved and distinguish among these modes. To understand the impact of convergent positive selection on neutral diversity at linked loci, we make use of the fact that hitchhiking can be modeled as an increase in the variance in neutral allele frequencies around a selected site within a population. We build on coalescent theory to show how shared hitchhiking events between subpopulations act to increase covariance in allele frequencies between subpopulations at loci near the selected site, and extend this theory under different models of migration and selection on the same standing variation. We incorporate this hitchhiking effect into a multivariate normal model of allele frequencies that also accounts for population structure. Based on this theory, we present a composite-likelihood-based approach that utilizes genomic data to identify loci involved in convergence, and distinguishes among alternate modes of convergent adaptation. We illustrate our method on genome-wide polymorphism data from two distinct cases of convergent adaptation. First, we investigate the adaptation for copper toxicity tolerance in two populations of the common yellow monkey flower, Mimulus guttatus We show that selection has occurred on an allele that has been standing in these populations prior to the onset of copper mining in this region. Lastly, we apply our method to data from four populations of the killifish, Fundulus heteroclitus, that show very rapid convergent adaptation for tolerance to industrial pollutants. Here, we identify a single locus at which both independent mutation events and selection on an allele shared via gene flow, either slightly before or during selection, play a role in adaptation across the species' range.

Adaptive responses to thermal stress in poikilotherms plays an important role in determining competitive ability and species distributions. Amino acid substitutions that affect protein stability and modify the thermal optima of orthologous proteins may be particularly important in this context. Here, we examine a set of 2,770 protein-coding genes to determine if proteins in a highly invasive heat tolerant blue mussel (Mytilus galloprovincialis) contain signals of adaptive increases in protein stability relative to orthologs in a more cold tolerant M. trossulus. Such thermal adaptations might help to explain, mechanistically, the success with which the invasive marine mussel M. galloprovincialis has displaced native species in contact zones in the eastern (California) and western (Japan) Pacific. We tested for stabilizing amino acid substitutions in warm tolerant M. galloprovincialis relative to cold tolerant M. trossulus with a generalized linear model that compares in silico estimates of recent changes in protein stability among closely related congeners. Fixed substitutions in M. galloprovincialis were 3,180.0 calories per mol per substitution more stabilizing at genes with both elevated dN/dS ratios and transcriptional responses to heat stress, and 705.8 calories per mol per substitution more stabilizing across all 2,770 loci investigated. Amino acid substitutions concentrated in a small number of genes were more stabilizing in M. galloprovincialis compared with cold tolerant M. trossulus. We also tested for, but did not find, enrichment of a priori GO terms in genes with elevated dN/dS ratios in M. galloprovincialis. This might indicate that selection for thermodynamic stability is generic across all lineages, and suggests that the high change in estimated protein stability that we observed in M. galloprovincialis is driven by selection for extra stabilizing substitutions, rather than by higher incidence of selection in a greater number of genes in this lineage. Nonetheless, our finding of more stabilizing amino acid changes in the warm adapted lineage is important because it suggests that adaption for thermal stability has contributed to M. galloprovincialis' superior tolerance to heat stress, and that pairing tests for positive selection and tests for transcriptional response to heat stress can identify candidates of protein stability adaptation.

Much of our understanding of the thermal physiology of intertidal organisms comes from experiments with animals acclimated under constant conditions and exposed to a single heat stress. In nature, however, the thermal environment is more complex. Aerial exposure and the unpredictable nature of thermal stress during low tides may be critical factors in defining the thermal physiology of intertidal organisms. In the fingered limpet, Lottia digitalis, we investigated whether upper temperature tolerance and thermal sensitivity were influenced by the pattern of fluctuation with which thermal stress was applied. Specifically, we examined whether there was a differential response (measured as cardiac performance) to repeated heat stress of a constant and predictable magnitude compared with heat stress applied in a stochastic and unpredictable nature. We also investigated differences in cellular metabolism and damage following immersion for insights into biochemical mechanisms of tolerance. Upper temperature tolerance increased with aerial exposure, but no significant differences were found between predictable treatments of varying magnitudes (13°C versus 24°C versus 32°C). Significant differences in thermal tolerance were found between unpredictable trials with different heating patterns. There were no significant differences among treatments in basal citrate synthase activity, glycogen content, oxidative stress or antioxidants. Our results suggest that aerial exposure and recent thermal history, paired with relief from high low-tide temperatures, are important factors modulating the capacity of limpets to deal with thermal stress.

Tardigrades are microscopic animals that survive a remarkable array of stresses, including desiccation. How tardigrades survive desiccation has remained a mystery for more than 250 years. Trehalose, a disaccharide essential for several organisms to survive drying, is detected at low levels or not at all in some tardigrade species, indicating that tardigrades possess potentially novel mechanisms for surviving desiccation. Here we show that tardigrade-specific intrinsically disordered proteins (TDPs) are essential for desiccation tolerance. TDP genes are constitutively expressed at high levels or induced during desiccation in multiple tardigrade species. TDPs are required for tardigrade desiccation tolerance, and these genes are sufficient to increase desiccation tolerance when expressed in heterologous systems. TDPs form non-crystalline amorphous solids (vitrify) upon desiccation, and this vitrified state mirrors their protective capabilities. Our study identifies TDPs as functional mediators of tardigrade desiccation tolerance, expanding our knowledge of the roles and diversity of disordered proteins involved in stress tolerance.

There is an accumulating body of evidence suggesting that the sub-zero Antarctic marine environment places physiological constraints on protein homeostasis. Levels of ubiquitin (Ub)-conjugated proteins, 20S proteasome activity and mRNA expression of many proteins involved in both the Ub tagging of damaged proteins as well as the different complexes of the 26S proteasome were measured to examine whether there is thermal compensation of the Ub-proteasome pathway in Antarctic fishes to better understand the efficiency of the protein degradation machinery in polar species. Both Antarctic (Trematomus bernacchii, Pagothenia borchgrevinki) and non-Antarctic (Notothenia angustata, Bovichtus variegatus) notothenioids were included in this study to investigate the mechanisms of cold adaptation of this pathway in polar species. Overall, there were significant differences in the levels of Ub-conjugated proteins between the Antarctic notothenioids and B. variegatus, with N. angustata possessing levels very similar to those of the Antarctic fishes. Proteasome activity in the gills of Antarctic fishes demonstrated a high degree of temperature compensation such that activity levels were similar to activities measured in their temperate relatives at ecologically relevant temperatures. A similar level of thermal compensation of proteasome activity was not present in the liver of two Antarctic fishes. Higher gill proteasome activity is likely due in part to higher cellular levels of proteins involved in the Ub-proteasome pathway, as evidenced by high mRNA expression of relevant genes. Reduced activity of the Ub-proteasome pathway does not appear to be the mechanism responsible for elevated levels of denatured proteins in Antarctic fishes, at least in the gills.