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Understanding how organisms adapt to changing environments is a core focus of research in evolutionary biology. One common mechanism is adaptive introgression, which has received increasing attention as a potential route to rapid adaptation in populations struggling in the face of ecological change, particularly global climate change. However, hybridization can also result in deleterious genetic interactions that may limit the benefits of adaptive introgression. Here, we used a combination of genome-wide quantitative trait locus mapping and differential gene expression analyses between the swordtail fish species Xiphophorus malinche and X. birchmanni to study the consequences of hybridization on thermotolerance. While these two species are adapted to different thermal environments, we document a complicated architecture of thermotolerance in hybrids. We identify a region of the genome that contributes to reduced thermotolerance in individuals heterozygous for X. malinche and X. birchmanni ancestry, as well as widespread misexpression in hybrids of genes that respond to thermal stress in the parental species, particularly in the circadian clock pathway. We also show that a previously mapped hybrid incompatibility between X. malinche and X. birchmanni contributes to reduced thermotolerance in hybrids. Together, our results highlight the challenges of understanding the impact of hybridization on complex ecological traits and its potential impact on adaptive introgression., (© 2022 John Wiley & Sons Ltd.)

Research conducted during the past two decades has demonstrated that biological invasions are excellent models of rapid evolution. Even so, characteristics of invasive populations such as a short time for recombination to assemble optimal combinations of alleles may occasionally limit adaptation to new environments. Here, we investigated such genetic constraints to adaptation in the invasive brown anole (Anolis sagrei)-a tropical ectotherm that was introduced to the southeastern United States, a region with a much colder climate than in its native Caribbean range. We examined thermal physiology for 30 invasive populations and tested for a climatic cline in cold tolerance. Also, we used genomics to identify mechanisms that may limit adaptation. We found no support for a climatic cline, indicating that thermal tolerance did not shift adaptively. Concomitantly, population genomic results were consistent with the occurrence of recombination cold spots that comprise more than half of the genome and maintain long-range associations among alleles in invasive populations. These genomic regions overlap with both candidate thermal tolerance loci that we identified using a standard genome-wide association test. Moreover, we found that recombination cold spots do not have a large contribution to population differentiation in the invasive range, contrary to observations in the native range. We suggest that limited recombination is constraining the contribution of large swaths of the genome to adaptation in invasive brown anoles. Our study provides an example of evolutionary stasis during invasion and highlights the possibility that reduced recombination occasionally slows down adaptation in invasive populations., (© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Thermal priming of reef corals can enhance their heat tolerance; however, the legacy effects of heat stress during parental brooding on larval resilience remain understudied. This study investigated whether preconditioning adult coral Pocillopora damicornis to high temperatures (29°C and 32°C) could better prepare their larvae for heat stress. Results showed that heat-acclimated adults brooded larvae with reduced symbiont density and shifted thermal performance curves. Reciprocal transplant experiments demonstrated higher bleaching resistance and better photosynthetic and autotrophic performance in heat-exposed larvae from acclimated adults compared to unacclimated adults. RNA-seq revealed strong cellular stress responses in larvae from heat-acclimated adults that could have been effective in rescuing host cells from stress, as evidenced by the widespread upregulation of genes involved in cell cycle and mitosis. For symbionts, a molecular coordination between light harvesting, photoprotection and carbon fixation was detected in larvae from heat-acclimated adults, which may help optimize photosynthetic activity and yield under high temperature. Furthermore, heat acclimation led to opposing regulations of symbiont catabolic and anabolic pathways and favoured nutrient translocation to the host and thus a functional symbiosis. Notwithstanding, the improved heat tolerance was paralleled by reduced light-enhanced dark respiration, indicating metabolic depression for energy saving. Our findings suggest that adult heat acclimation can rapidly shift thermal tolerance of brooded coral larvae and provide integrated physiological and molecular evidence for this adaptive plasticity, which could increase climate resilience. However, the metabolic depression may be maladaptive for long-term organismal performance, highlighting the importance of curbing carbon emissions to better protect corals., (© 2022 John Wiley & Sons Ltd.)

Adaptation to environmental variability is a prerequisite for species' persistence in their natural environments. With climate change predicted to increase the frequency and severity of temperature fluctuations, ectothermic organisms may increasingly depend on acclimation capacity to accommodate thermal variability. To elucidate the molecular basis of fluctuating temperature-induced phenotypic plasticity, we investigated heat tolerance and the mechanisms induced by acclimation to thermal variability as compared to those seen at constant temperature. We ran genome-wide transcriptomic analysis on Drosophila melanogaster subjected to acclimation at constant (19 ± 0°C) and fluctuating (19 ± 8°C) temperatures and contrasted the induction of molecular mechanisms in adult males, adult females and larvae. We found life stage- and sex-specific dynamics of the acclimation responses to fluctuating temperatures. Adult flies exposed to temperature fluctuations showed a constitutive improvement in heat tolerance while heat tolerance of larvae tracked thermal fluctuations. A constitutive down-regulation of gene expression was observed for several genes in the larvae exposed to fluctuations. Our results for adult females showed that, for several genes, fluctuating temperature acclimation resulted in canalization of gene expression. Both transcriptional and post-transcriptional machinery were greatly affected by fluctuations in adult males. Gene ontology analysis showed enrichment of the heat stress response involving several major heat shock proteins in both larvae and adults exposed to fluctuating temperatures, even though fluctuations were in a benign range of temperatures. Finally, molecular mechanisms related to environmental sensing seem to be an important component of insect responses to thermal variability., (© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

The ubiquitous human commensal Escherichia coli has been well investigated through its model representative E. coli K-12. In this work, we initially characterized E. coli Fec10, a recently isolated human commensal strain of phylogroup A/sequence type ST10. Compared to E. coli K-12, the 4.88 Mbp Fec10 genome is characterized by distinct single-nucleotide polymorphisms and acquisition of genomic islands. In addition, E. coli Fec10 possesses a 155.86 kbp IncY plasmid, a composite element based on phage P1. pFec10 harbours multiple cargo genes such as coding for a tetrathionate reductase and its corresponding regulatory two-component system. Among the cargo genes is also the Transmissible Locus of Protein Quality Control (TLPQC), which mediates tolerance to lethal temperatures in bacteria. The disaggregase ClpG GI of TLPQC constitutes a major determinant of the thermotolerance of E. coli Fec10. We confirmed stand-alone disaggregation activity, but observed distinct biochemical characteristics of ClpG GI-Fec10 compared to the nearly identical Pseudomonas aeruginosa ClpG GI-SG17M. Furthermore, we noted a unique contribution of ClpG GI-Fec10 to the exquisite thermotolerance of E. coli Fec10, suggesting functional differences between both disaggregases in vivo. Detection of thermotolerance in 10% of human commensal E. coli isolates hints to the successful establishment of food-borne heat-resistant strains in the human gut., (© 2020 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.)

Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand how D. trenchii modulates coral gene expression by manipulating symbiont communities in Montastraea cavernosa to produce replicate ramets containing D. trenchii together with paired ramets of these same genets (n = 3) containing Cladocopium C3 symbionts. We then examined differences in global gene expression between corals hosting Durusdinium and Cladocopium under control temperatures, and in response to short-term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%-14% of the transcriptional variance. Corals with D. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals with Cladocopium. Unexpectedly, these changes were similar to those observed in Cladocopium-dominated corals in response to heat stress, suggesting that thermotolerant D. trenchii may cause corals to increase expression of heat stress-responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containing D. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts., (© 2020 John Wiley & Sons Ltd.)

Investigating the history of natural selection among closely related species can elucidate how genomes diverge in response to disparate environmental pressures. Molecular evolutionary approaches can be integrated with knowledge of gene functions to examine how evolutionary divergence may affect ecologically relevant traits such as temperature tolerance and species distribution limits. Here, we integrate transcriptome-wide analyses of molecular evolution with knowledge from physiological studies to develop hypotheses regarding the functional classes of genes under positive selection in one of the world's most widespread invasive species, the warm-tolerant marine mussel Mytilus galloprovincialis. Based on existing physiological information, we test the hypothesis that genomic functions previously linked to divergent temperature adaptation at the whole-organism level show accelerated molecular divergence between warm-adapted M. galloprovincialis and cold-adapted congeners. Combined results from codon model tests and analyses of polymorphism and divergence reveal that divergent selection has affected genomic functions previously associated with species-specific expression responses to heat stress, namely oxidative stress defence and cytoskeletal stabilization. Examining specific loci implicated in thermal tolerance among Mytilus species (based on interspecific biochemical or expression patterns), we find close functional similarities between known thermotolerance candidate genes under positive selection and positively selected loci under predicted genomic functions (those associated with divergent expression responses). Taken together, our findings suggest a contribution of temperature-dependent selection in the molecular divergence between warm- and cold-adapted Mytilus species that is largely consistent with results from physiological studies. More broadly, this study provides an example of how independent experimental evidence from ecophysiological investigations can inform evolutionary hypotheses about molecular adaptation in closely related nonmodel species., (© 2019 John Wiley & Sons Ltd.)

Reef-building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for corals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef-builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow-sense heritability of variation in bleaching responses, revealing that variation in these responses was highly heritable (h 2  = 0.58). This suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. We further investigated the functional basis for this variation using genomic and transcriptomic approaches. We used a publicly available genetic linkage map and genome assembly to map markers associated with bleaching responses, identifying twelve markers associated with variation in bleaching responses. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial differences in transcriptional stress responses between heat-tolerant and heat-susceptible corals. Together, our findings contribute to the growing body of evidence that natural populations of corals possess genetic variation in thermal stress responses that may potentially support adaptive responses to rising ocean temperatures., (© 2019 John Wiley & Sons Ltd.)

Domestic species such as cattle (Bos taurus taurus and B. t. indicus) represent attractive biological models to characterize the genetic basis of short-term evolutionary response to climate pressure induced by their post-domestication history. Here, using newly generated dense SNP genotyping data, we assessed the structuring of genetic diversity of 21 autochtonous cattle breeds from the whole Mediterranean basin and performed genome-wide association analyses with covariables discriminating the different Mediterranean climate subtypes. This provided insights into both the demographic and adaptive histories of Mediterranean cattle. In particular, a detailed functional annotation of genes surrounding variants associated with climate variations highlighted several biological functions involved in Mediterranean climate adaptation such as thermotolerance, UV protection, pathogen resistance or metabolism with strong candidate genes identified (e.g., NDUFB3, FBN1, METTL3, LEF1, ANTXR2 and TCF7). Accordingly, our results suggest that main selective pressures affecting cattle in Mediterranean area may have been related to variation in heat and UV exposure, in food resources availability and in exposure to pathogens, such as anthrax bacteria (Bacillus anthracis). Furthermore, the observed contribution of the three main bovine ancestries (indicine, European and African taurine) in these different populations suggested that adaptation to local climate conditions may have either relied on standing genomic variation of taurine origin, or adaptive introgression from indicine origin, depending on the local breed origins. Taken together, our results highlight the genetic uniqueness of local Mediterranean cattle breeds and strongly support conservation of these populations., (© 2019 John Wiley & Sons Ltd.)

Species extinction rates are many times greater than the direst predictions made two decades ago by environmentalists, largely because of human impact. Major concerns are associated with the predicted higher recurrence and severity of extreme events, such as heat waves. Although tolerance to these extreme events is instrumental to species survival, little is known whether and how it evolves in natural populations, and to what extent it is affected by other environmental stressors. Here, we study physiological and molecular mechanisms of thermal tolerance over evolutionary times in multifarious environments. Using the practice of "resurrection ecology" on the keystone grazer Daphnia magna, we quantified genetic and plastic differences in physiological and molecular traits linked to thermal tolerance in historical and modern genotypes of the same population. This population experienced an increase in average temperature and occurrence of heat waves, in addition to dramatic changes in water chemistry, over five decades. On genotypes resurrected across the five decades, we measured plastic and genetic differences in CT max , body size, Hb content and differential expression of four heat shock proteins after exposure to temperature as single stress and in combination with food levels and insecticide loads. We observed evolution of the critical thermal maximum and plastic response in body size, HSP expression and Hb content over time in a warming only scenario. Molecular and physiological responses to extreme temperature in multifarious environments were not predictable from the response to warming alone. Underestimating the effect of multiple stressors on thermal tolerance can lead to wrong estimates of species evolvability and persistence., (© 2018 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd.)

We found that mutations that increased the transcription of the mgtCBR (Mg 2+ transport-related) operon conferred increased thermotolerance on this organism. The 5' leader of the mgtCBR mRNA contains two short open reading frames (ORFs), mgtM and mgtP, whose translation regulates the expression of the mgtCBR operon by a mechanism that is similar to attenuation in amino acid biosynthetic operons. We obtained two types of mutations that resulted in elevated transcription of the operon: defects in the mgtM ribosome-binding site, impairing the translation of this ORF and deletions encompassing the stop codon of mgtM that extend the translation of this ORF across a downstream Rho termination site. These mgtM mutations give further insights into the mechanism of the transcriptional control of the mgtCBR operon that we discuss in this work. We show that the increased thermotolerance requires elevated expression of the mgtC gene, but functional mgtB and mgtR, which respectively encode an Mg 2+ transporter and a regulatory protein, are dispensable for this response. MgtC has been shown to have complex functions, including a requirement for virulence, flagella-independent motility and synthesis of cellulose and we now found that it has a role in the regulation of thermotolerance., (© 2018 John Wiley & Sons Ltd.)

As climate changes, sea surface temperature anomalies that negatively impact coral reef organisms continue to increase in frequency and intensity. Yet, despite widespread coral mortality, genetic diversity remains high even in those coral species listed as threatened. While this is good news in many ways, it presents a challenge for the development of biomarkers that can identify resilient or vulnerable genotypes. Taking advantage of three coral restoration nurseries in Florida that serve as long-term common garden experiments, we exposed over 30 genetically distinct Acropora cervicornis colonies to hot and cold temperature shocks seasonally and measured pooled gene expression responses using RNAseq. Targeting a subset of 20 genes, we designed a high-throughput qPCR array to quantify expression in all individuals separately under each treatment with the goal of identifying predictive and/or diagnostic thermal stress biomarkers. We observed extensive transcriptional variation in the population, suggesting abundant raw material is available for adaptation via natural selection. However, this high variation made it difficult to correlate gene expression changes with colony performance metrics such as growth, mortality and bleaching susceptibility. Nevertheless, we identified several promising diagnostic biomarkers for acute thermal stress that may improve coral restoration and climate change mitigation efforts in the future., (© 2018 John Wiley & Sons Ltd.)

Evolutionary rescue (ER) occurs when populations, which have declined due to rapid environmental change, recover through genetic adaptation. The success of this process and the evolutionary trajectory of the population strongly depend on the rate of environmental change. Here we investigated how different rates of temperature increase (from 23 to 32 °C) affect population persistence and evolutionary change in experimental microcosms of the protozoan Paramecium caudatum. Consistent with theory on ER, we found that those populations experiencing the slowest rate of temperature increase were the least likely to become extinct and tended to be the best adapted to the new temperature environment. All high-temperature populations were more tolerant to severe heat stress (35, 37 °C), indicating a common mechanism of heat protection. High-temperature populations also had superior growth rates at optimum temperatures, leading to the absence of a pattern of local adaptation to control (23 °C) and high-temperature (32 °C) environments. However, high-temperature populations had reduced growth at low temperatures (5-9 °C), causing a shift in the temperature niche. In part, the observed evolutionary change can be explained by selection from standing variation. Using mitochondrial markers, we found complete divergence between control and high-temperature populations in the frequencies of six initial founder genotypes. Our results confirm basic predictions of ER and illustrate how adaptation to an extreme local environment can produce positive as well as negative correlated responses to selection over the entire range of the ecological niche., (© 2017 John Wiley & Sons Ltd.)

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long-term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm- and cold-adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST-linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna., (© 2017 John Wiley & Sons Ltd.)