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Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana

Because earth is currently experiencing unprecedented climate change, it is important to predict how species will respond to it. However, geographically-explicit predictive studies frequently ignore that species are comprised of genetically diverse individuals that can vary in their degree of adaptation to extreme local environments; properties that will determine the species ability to withstand climate change. Because an increase in extreme drought events is expected to challenge plant communities with global warming, we carried out a greenhouse experiment to investigate which genetic variants predict surviving an extreme drought event and how those variants are distributed across Eurasian Arabidopsis thaliana individuals. Genetic variants conferring higher drought survival showed signatures of polygenic adaptation, and were more frequently found in Mediterranean and Scandinavian regions. Using geoenvironmental models, we predicted that Central European populations might lag behind in adaptation by the end of the 21st century. Further analyses showed that a population decline could nevertheless be compensated by natural selection acting efficiently over standing variation or by migration of adapted individuals from populations at the margins of the species distribution. These findings highlight the importance of within-species genetic heterogeneity in facilitating an evolutionary response to a changing climate.\n\nOne-sentence summary\"Future genetic changes in A. thaliana populations can be forecast by combining climate change models with genomic predictions based on experimental phenotypic data.\"

evolutionary biology

The genomic footprint of climate adaptation in Chironomus riparius

The gradual heterogeneity of climatic factors pose varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift, and adaptation to non-clinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool-Seq data, and population genetic modelling. Common-garden experiments revealed a positive correlation of population growth rates corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an FST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in other studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.

evolutionary biology

Evolution Of Hierarchy In Bacterial Metabolic Networks

BackgroundIn self-organized systems, the concept of flow hierarchy is a useful way to characterize the movement of information throughout a network. Hierarchical network organizations are shown to arise when there is a cost of maintaining links in the network. A similar constraint exists in metabolic networks, where costs come from reduced efficiency of nonspecific enzymes or from producing unnecessary enzymes. Previous analyses of bacterial metabolic networks have been used to predict the minimal nutrients that a bacterium needs to grow, its mutualistic relationships with other bacteria, and its major ecological niche. Using flow hierarchy, we can also infer the tradeoffs between growth rate and metabolic efficiency that bacteria make given their environmental constraints.\n\nResultsUsing a comparative approach on 2,935 bacterial metabolic networks, we show that flow hierarchy in bacterial metabolic networks tracks a fundamental tradeoff between growth rate and biomass production, and reflects a bacteriums realized ecological strategy. Additionally, by inferring the ancestral metabolic networks, we find that hierarchy decreases with distance from the root of the tree, suggesting the important pressure of increased growth rate relative to efficiency in the face of competition.\n\nConclusionsJust as hierarchical character is an important structural property in efficiently engineered systems, it also evolves in self-organized bacterial metabolic networks, reflects the life-history strategies of those bacteria, and plays an important role in network organization and efficiency.

evolutionary biology

Neuronal Patterning Of The Tubular Collar Cord Is Highly Conserved Among Enteropneusts But Dissimilar To The Chordate Neural Tube

The dorsal neural tube of chordates and the ventral nerve cord of annelids exhibit a similar molecular mediolateral architecture. Accordingly, the presence of such a complex nervous system (CNS) has been proposed for their last common ancestor. Members of Enteropneusta, a group of non-chordate deuterostomes, possess a less complex CNS including a hollow neural tube, whereby homology to its chordate counterpart remains elusive. Since the majority of data on enteropneusts stem from Saccoglossus kowalevskii, a derived direct-developer, we investigated expression of key neuronal patterning genes in the indirect-developer Balanoglossus misakiensis.\n\nThe collar cord of B. misakiensis shows anterior Six3/6 and posterior Otx + engrailed expression, in a region corresponding to the chordate brain. Neuronal Nk2.1/Nk2.2 expression is absent. Interestingly, we found median Dlx and lateral Pax6 expression domains, i.e., a condition that is reversed compared to chordates.\n\nComparative analyses reveal that CNS patterning is highly conserved among enteropneusts. BmiDlx and BmiPax6 have no corresponding expression domains in the chordate brain, which may be indicative of independent acquisition of a tubular CNS in Enteropneusta and Chordata. Moreover, mediolateral architecture varies considerably among chordates and enteropneusts, questioning the presence of a vertebrate-like patterned nervous system in the last common deuterostome ancestor.

evolutionary biology

Temporal fitness fluctuations in experimental Arabidopsis thaliana populations

Understanding the genetics of lifetime fitness is crucial to understand a species ecological preferences and ultimately predict its ability to cope with novel environmental conditions. Yet, there is a dearth of information regarding the impact of the ecological variance experienced by natural populations on expressed phenotypic and fitness differences. Here, we follow the natural dynamics of experimental A. thaliana populations over 5 successive plantings whose timing was determined by the natural progression of the plants life cycle and disentangle the environmental and genetic factors that drive plant ecological performance at a given locality. We show that, at the intermediate latitude where the experiment was conducted, a given genotype can experience different life cycles across successive seasons. Lifetime fitness across these seasons varied strongly, with a fall planting yielding 36-fold higher fitness compared to a spring planting. In addition, the actual life-stage at which plant overwinter oscillated across years, depending on the timing of the end of the summer season. We observed a rare but severe fitness differential after inadequate early flowering in one of the five planting. Substrate variation played a comparatively minor role, but also contributed to modulate the magnitude of fitness differentials between genotypes. Finally, reciprocal introgressions on chromosome 4 demonstrated that the fitness effect of a specific chromosomal region is strongly contingent on micro-geographic and seasonal fluctuations. Our study contributes to emphasize the extent to which the fitness impact of phenotypic traits and the genes that encode them in the genome can fluctuate. Experiments aiming at dissecting the molecular basis of local adaptation must apprehend the complexity introduced by temporal fluctuations because they massively affect the expression of phenotype and fitness differences.

evolutionary biology

Selective sweep analysis using village dogs highlights the pivotal role of the neural crest in dog domestication

BackgroundDogs (Canis lupus familiaris) were domesticated from gray wolves between 10-40 kya in Eurasia, yet details surrounding the process of domestication remain unclear. The vast array of phenotypes exhibited by dogs mirror other domesticated animal species, a phenomenon known as the Domestication Syndrome. Here, we use signatures persisting in the dog genome to identify genes and pathways altered by the intensive selective pressures of domestication.\n\nResultsWe identified 246 candidate domestication regions containing 10.8Mb of genome sequence and 178 genes through whole-genome SNP analysis of 43 globally distributed village dogs and 10 wolves. Comparisons with ancient dog genomes suggest that these regions reflect signatures of domestication rather than breed formation. The strongest hit is located in the Retinoic Acid-Induced 1 (RAI1) gene, mutations of which cause Smith-Magenis syndrome. The identified regions contain a significant enrichment of genes linked to neural crest cell migration, differentiation and development. Read depth analysis suggests that copy number variation played a minor role in dog domestication.\n\nConclusionOur results indicate that phenotypes distinguishing domesticated dogs from wolves, such as tameness, smaller jaws, floppy ears, and diminished craniofacial development, are determined by genes which act early in embryogenesis. These differences are all phenotypes of the Domestication Syndrome, which can be explained by decreases in neural crest cells at these sites. We propose that initial selection during early dog domestication was for behavior, a trait also influenced by genes which act in the neural crest, which secondarily gave rise to the phenotypes of modern dogs.

evolutionary biology

MSAP In Tiger Snakes: Island Populations Are Epigenetically More Divergent

Research on changes in phenotypic plasticity within wild animal populations is centuries old, however far fewer studies have investigated the role that epigenetics play in the development or persistence of natural variation in response to environmental change. Tiger snakes (Notechis scutatus) are an ideal study organism to investigate the link between epigenetics and phenotypic responses to environmental change, as they live on a range of offshore islands with different environments and prey types while exhibiting gigantism and dwarfism in body and head size. In this study, we have generated methylation sensitive amplified polymorphism (MSAP) data and found that, in general, Tiger Snakes are more epigenetically differentiated than genetically differentiated. Each island group has a distinctive epigenetic signal, suggesting the Tiger Snakes on each island group have adapted to their specific environment. This is also supported by the strong positive relationship between epigenetic differentiation and isolation age, as well as between epigenetic/genetic signal and both temperature and precipitation. The Tiger Snakes from Kangaroo Island, which has a complex landscape/environment like the mainland rather than the simple landscape/environment of each of the smaller islands, are both genetically and epigenetically more like the mainland. As the MSAP loci are randomly distributed across the genome, we believe a closer examination of the epigenetic modifications near genes involved in growth, development, and lipid metabolism will allow us to investigate the epigenetic basis for the natural variation in head size and body size on the islands.

evolutionary biology

The physical boundaries of public goods cooperation between surface-attached bacterial cells

Bacteria secrete a variety of compounds important for nutrient scavenging, competition mediation and infection establishment. While there is a general consensus that secreted compounds can be shared and therefore have social consequences for the bacterial collective, we know little about the physical limits of such bacterial social interactions. Here, we address this issue by studying the sharing of iron-scavenging siderophores between surface-attached microcolonies of the bacterium Pseudomonas aeruginosa. Using single-cell fluorescent microscopy, we show that siderophores, secreted by producers, quickly reach non-producers within a range of 100 m, and significantly boost their fitness. Producers in turn respond to variation in sharing efficiency by adjusting their pyoverdine investment levels. These social effects wane with larger cell-to-cell distances and on hard surfaces. Thus, our findings reveal the boundaries of compound sharing, and show that sharing is particularly relevant between nearby yet physically separated bacteria on soft surfaces, matching realistic natural conditions such as those encountered in soft tissue infections.

evolutionary biology

Pan-genome and phylogeny of Bacillus cereus sensu lato

BackgroundBacillus cereus sensu lato (s. l.) is an ecologically diverse bacterial group of medical and agricultural significance. In this study, I use publicly available genomes to characterize the B. cereus s. l. pan-genome and perform the largest phylogenetic and population genetic analyses of this group to date in terms of the number of genes and taxa included. With these fundamental data in hand, I identify genes associated with particular phenotypic traits (i.e., \"pan-GWAS\" analysis), and quantify the degree to which taxa sharing common attributes are phylogenetically clustered.\n\nMethodsA rapid k-mer based approach (Mash) was used to create reduced representations of selected Bacillus genomes, and a fast distance-based phylogenetic analysis of this data (FastME) was performed to determine which species should be included in B. cereus s. l. The complete genomes of eight B. cereus s. l. species were annotated de novo with Prokka, and these annotations were used by Roary to produce the B. cereus s. l. pan-genome. Scoary was used to associate gene presence and absence patterns with various phenotypes. The orthologous protein sequence clusters produced by Roary were filtered and used to build HaMStR databases of gene models that were used in turn to construct phylogenetic data matrices. Phylogenetic analyses used RAxML, DendroPy, ClonalFrameML, PAUP*, and SplitsTree. Bayesian model-based population genetic analysis assigned taxa to clusters using hierBAPS. The genealogical sorting index was used to quantify the phylogenetic clustering of taxa sharing common attributes.\n\nThe B. cereus s. l. pan-genome currently consists of {approx}60,000 genes, {approx}600 of which are \"core\" (common to at least 99% of taxa sampled). Pan-GWAS analysis revealed genes associated with phenotypes such as isolation source, oxygen requirement, and ability to cause diseases such as anthrax or food poisoning. Extensive phylogenetic analyses using an unprecedented amount of data produced phylogenies that were largely concordant with each other and with previous studies. Phylogenetic support as measured by bootstrap probabilities increased markedly when all suitable pan-genome data was included in phylogenetic analyses, as opposed to when only core genes were used. Bayesian population genetic analysis recommended subdividing the three major clades of B. cereus s. l. into nine clusters. Taxa sharing common traits and species designations exhibited varying degrees of phylogenetic clustering.

evolutionary biology

Plant organ evolution revealed by phylotranscriptomics in Arabidopsis

The evolution of species phenotypes occurs through changes both in protein sequence and gene expression levels. Though much of plant morphological evolution can be explained by changes in gene expression, examining its evolution has challenges. To gain a new perspective on organ evolution in plants, we applied a phylotranscriptomics approach. We combined a phylostratigraphic approach with gene expression based on the strand-specific RNA-seq data from seedling, floral bud, and root of 19 Arabidopsis thaliana accessions to examine the age and sequence divergence of transcriptomes from these organs and how they adapted over time. Our results indicate that, among the sense and antisense transcriptomes of these organs, the sense transcriptomes of seedlings are the evolutionarily oldest across all accessions and are the most conserved in amino acid sequence for most accessions. In contrast, among the sense transcriptomes from these same organs, those from floral bud are evolutionarily youngest and least conserved in sequence for most accessions. Different organs have adaptive peaks at different stages in their evolutionary history, however, from the Magnoliophyta stage to the Brassicale stage, all three organs show a common adaptive signal. Our research is significant because it offers novel evolutionary insight on plant organs revealed by phylotranscriptomics.

evolutionary biology

Ecological drivers of body size evolution and sexual size dimorphism in short-horned grasshoppers (Orthoptera: Acrididae)

Sexual size dimorphism (SSD) is widespread and variable in nature. Although female-biased SSD predominates among insects, the proximate ecological and evolutionary factors promoting this phenomenon remain largely unstudied. Here, we employ modern phylogenetic comparative methods on 8 subfamilies of Iberian grasshoppers (85 species) to examine the validity of different models of evolution of body size and SSD and explore how they are shaped by a suite of ecological variables (habitat specialization, substrate use, altitude) and/or constrained by different evolutionary pressures (female fecundity, strength of sexual selection, length of the breeding season). Body size disparity primarily accumulated late in the history of the group and did not follow a Brownian motion pattern, indicating the existence of directional evolution for this trait. We found support for the converse of Renschs rule across all taxa but not within the two most speciose subfamilies (Gomphocerinae and Oedipodinae), which showed an isometric pattern. Our results do not provide support for the fecundity or sexual selection hypotheses and we did not find evidence for significant effects of habitat use. Contrary to that expected, we found that species with narrower reproductive window are less dimorphic in size than those that exhibit a longer breeding cycle, suggesting that male protandry cannot solely account for the evolution of female-biased SSD in Orthoptera. Our study highlights the need to consider alternatives to the classical evolutionary hypotheses when trying to explain why in certain insect groups males remain small.

evolutionary biology

Distinguishing among modes of convergent adaptation using population genomic data

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.

evolutionary biology

Identification And Characterization Of Domesticated Bacterial Transposases

Selfish genetic elements (SGEs), such as insertion sequences (ISs) and transposons are found in most genomes. Transposons are usually identifiable by their high copy number within genomes. In contrast REP associated tyrosine transposases (RAYTs), a recently described class of bacterial transposase, are typically present at just one copy per genome. This suggests that RAYTs no longer copy themselves and thus they no longer function as a typical transposase. Motivated by this possibility we interrogated thousands of fully sequenced bacterial genomes in order to determine patterns of RAYT diversity, their distribution across chromosomes and accessory elements, and rate of duplication. RAYTs encompass exceptional diversity and are divisible into at least five distinct groups. They possess features more similar to housekeeping genes than insertion sequences, are predominantly vertically transmitted and have persisted through evolutionary time to the point where they are now found in 24% of all species for which at least one fully sequenced genome is available. Overall, the genomic distribution of RAYTs suggests that they have been co-opted by host genomes to perform a function that benefits the host cell.

evolutionary biology

Pathogenic Amino Acid Variants In Mitochondrial Proteins More Frequently Arise In Lineages Closely Related To Human Than In Distantly Related Lineages

Propensities for different amino acids within a protein site change in the course of evolution, so that an amino acid deleterious in a particular species may be acceptable at the same site in a different species. Here, we study the amino acid-changing variants in human mitochondrial genes, and analyze their occurrence in non-human species. We show that substitutions giving rise to the human amino acid variant tend to occur in lineages closely related to human more frequently than in more distantly related lineages, indicating that a human variant is more likely to be deleterious in more distant species. Unexpectedly, amino acids corresponding to pathogenic alleles in humans also more frequently originate at more closely related lineages. Therefore, a pathogenic variant still tends to be more acceptable in human mitochondria than a variant that may only be fit after a substantial perturbation of the protein structure.\n\nSignificanceHomologous proteins can carry different amino acids at the same position in different species. These changes can be neutral, or can reflect differences in the pressure of selection on these sites. We hypothesized that amino acids observable in human population appear on average more frequently in close than in distant human relatives. For mitochondrial proteins, we observe this for both frequent and rare human alleles. Unexpectedly, substitutions that would be pathogenic in humans also more frequently appear in species more closely related to humans than in distantly related ones. Therefore, despite their pathogenicity, these variants are on average more acceptable in humans than other amino acids that were observed at this site in distantly related species.

evolutionary biology

Weak epistasis may drive adaptation in recombining bacteria

The impact of epistasis on the evolution of multilocus traits depends on recombination. Population genetic theory has been largely developed for eukaryotes, many of which recombine so frequently that epistasis between polymorphisms has not been considered to play a large role in adaptation and has been compared to the fleeting influence of non-heritable effects. Many bacteria also recombine, some to the degree that their populations are described as panmictic or freely recombining. However, whether this recombination is sufficient to limit the ability of selection to act on epistatic contributions to fitness is unknown. We create a sensitive method to quantify homologous recombination in five bacterial pathogens and use these parameter estimates in a multilocus model of bacterial evolution with additive and epistatic effects. We find that even for highly recombining species (e.g. Streptococcus pneumoniae or Helicobacter pylori), selection may act on the cumulative effects of weak (as well as strong) interactions between distant mutations since homologous recombination typically transfers only short segments. Furthermore, whether selection acts more efficiently on physically proximal loci depends on the average recombination tract length. Epistasis may thus play an important role in the adaptive evolution of bacteria and, unlike in eukaryotes, does not need to be strong, involve near loci, or require specific metapopulation dynamics.

evolutionary biology

Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention

Hybridization and polyploidy followed by genome-wide diploidization significantly impacted the diversification of land plants. The ancient At- whole-genome duplication (WGD) preceded the diversification of crucifers (Brassicaceae). Some genera and tribes also experienced younger, mesopolyploid WGDs concealed by subsequent genome diploidization. Here we tested if multiple base chromosome numbers originated due to genome diploidization after independent mesopolyploid WGDs and how diploidization impacted post-polyploid gene retention. Sixteen species representing ten Brassicaceae tribes were analyzed by comparative chromosome painting and/or whole-transcriptome analysis of gene age distributions and phylogenetic analyses of gene duplications. Overall, we found evidence for at least 13 independent mesopolyploidies followed by different degrees of diploidization across the Brassicaceae. New mesotetraploid events were uncovered for tribes Anastaticeae, Iberideae and Schizopetaleae, and mesohexaploid WGDs for Cochlearieae and Physarieae. In contrast, we found convergent patterns of gene retention and loss among these independent WGDs. Our combined analyses of Brassicaceae genomic data indicate that the extant chromosome number variation in many plant groups, and especially polybasic but monophyletic taxa, can result from clade-specific genome duplications followed by diploidization. Our observation of parallel gene retention and loss across multiple independent WGDs provides one of the first multi-species tests that post-polyploid genome evolution is predictable.\n\nSignificance statementOur data show that multiple base chromosome numbers in some Brassicaceae clades originated due to genome diploidization following multiple independent whole-genome duplications (WGD). The parallel gene retention/loss across independent WGDs and diploidizations provides one of the first tests that post-polyploid genome evolution is predictable.

evolutionary biology

Regulatory remodeling in the allo-tetraploid frog Xenopus laevis

BackgroundGenome duplication has played a pivotal role in the evolution of many eukaryotic lineages, including the vertebrates. The most recent vertebrate genome duplication is that in Xenopus laevis, resulting from the hybridization of two closely related species about 17 million years ago [1]. However, little is known about the consequences of this duplication at the level of the genome, the epigenome and gene expression.\n\nResultsOf the parental subgenomes, S chromosomes have degraded faster than L chromosomes ever since the genome duplication and until the present day. Deletions appear to have the largest effect on pseudogene formation and loss of regulatory regions. Deleted regions are enriched for long DNA repeats and the flanking regions have high alignment scores, suggesting that non-allelic homologous recombination (NAHR) has played a significant role in the loss of DNA. To assess innovations in the X. laevis subgenomes we examined p300 (Ep300)-bound enhancer peaks that are unique to one subgenome and absent from X. tropicalis. A large majority of new enhancers are comprised of transposable elements. Finally, to dissect early and late events following interspecific hybridization, we examined the epigenome and the enhancer landscape in X. tropicalis x X. laevis hybrid embryos. Strikingly, young X. tropicalis DNA transposons are derepressed and recruit p300 in hybrid embryos.\n\nConclusionsThe results show that erosion of X. laevis genes and functional regulatory elements is associated with repeats and NAHR, and furthermore that young repeats have also contributed to the p300-bound regulatory landscape following hybridization and whole genome duplication.

evolutionary biology

Disparate patterns of thermal adaptation between life stages in temperate vs. tropical populations of Drosophila melanogaster

Many terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioral thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. Average maximum temperature of the warmest month of the year predicted embryonic thermal tolerance in tropical but not temperate sites. We further report that embryos live closer to their upper thermal limits than adultso--i.e., thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting dominance of heat-tolerant alleles. Together our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages in order to better predict adaptive limits.\n\nImpact SummaryClimate change may threaten the extinction of many ectothermic species, unless populations can evolutionarily adapt to rising temperatures. Natural selection should favor individuals with higher heat tolerances in hotter environments. But recent studies have found that individuals from hot and cold places often have similar heat tolerances. This pattern may indicate that the evolution of heat tolerance is constrained. If this were true, then it would have dire consequences for species persistence under novel thermal conditions.\n\nAn alternative explanation for lack of variation in heat tolerance is that mobile organisms dont need higher heat tolerances to survive in hotter places. The majority of studies have focused on heat tolerance of the adult life stage. Yet, adults in many species are mobile organisms that can avoid extreme heat by seeking shelter in cooler microhabitats (e.g., shaded locations). In contrast, immobile life stages (e.g., insect eggs) cannot behaviorally avoid extreme heat. Thus, mobile and immobile life stages may face different thermal selection pressures that lead to disparate patterns of thermal adaptation across life stages.\n\nHere, we compared heat tolerances of fruit fly adults and eggs (Drosophila melanogaster) from populations in temperate North America and tropical locations around the globe. Consistent with previous studies, we found no differences among populations in adult heat tolerance. However, eggs from tropical flies were consistently more heat tolerant than eggs from North American flies. Further, eggs had lower heat tolerance than adults. Consequently, fly eggs in the hotter tropics may experience heat death more frequently than adult flies later in life. This may explain why patterns of divergence in heat tolerance were decoupled across life stages. These patterns indicate that thermal adaptation may be life-stage-specific and suggest that future work should characterize thermal traits across life stages to better understand the evolution of thermal limits.

evolutionary biology