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In long-lived tree populations, when environmental change outpaces rates of evolutionary adaptation, plasticity in traits related to stress tolerance, dormancy, and dispersal may be vital for preventing extinction. While a population's genetic background partly determines its ability to adapt to a changing environment, so too do the many types of epigenetic modifications that occur within and among populations, which vary on timescales orders of magnitude faster than the emergence of new beneficial alleles. Consequently, phenotypic plasticity driven by epigenetic modification may be especially critical for sessile, long-lived organisms such as trees that must rely on this plasticity to keep pace with rapid anthropogenic environmental change. While studies have reported large effects of DNA methylation, histone modification, and non-coding RNAs on the expression of stress-tolerance genes and resulting phenotypic responses, little is known about the role of these effects in non-model plants and particularly in trees. Here, we review new findings in plant epigenetics with particular relevance to the ability of trees to adapt to or escape stressors associated with rapid climate change. Such findings include specific epigenetic influences over drought, heat, and salinity tolerance, as well as dormancy and dispersal traits. We also highlight promising findings concerning transgenerational inheritance of an epigenetic 'stress memory' in plants. As epigenetic information is becoming increasingly easy to obtain, we close by outlining ways in which ecologists can use epigenetic information better to inform population management and forecasting efforts. Understanding the molecular mechanisms behind phenotypic plasticity and stress memory in tree species offers a promising path towards a mechanistic understanding of trees' responses to climate change.

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Numerous studies have shown that neuronal representations in sensory pathways are far from static but are instead strongly shaped by the complex properties of the sensory inputs they receive. Adaptation dynamically shapes the neural signaling that underlies our perception of the world yet remains poorly understood. We investigated rapid adaptation across timescales from hundreds of milliseconds to seconds through simultaneous multi-electrode recordings from the ventro-posteromedial nucleus of the thalamus (VPm) and layer 4 of the primary somatosensory cortex (S1) in male and female anesthetized mice in response to controlled, persistent whisker stimulation. Observations in VPm and S1 reveal a degree of adaptation that progresses through the pathway. Signatures of two distinct timescales of rapid adaptation in the firing rates of both thalamic and cortical neuronal populations were revealed, also reflected in the synchrony of the thalamic population and in the thalamocortical synaptic efficacy that was measured in putatively monosynaptically connected thalamocortical pairs. Controlled optogenetic activation of VPm further demonstrated that the longer timescale adaptation observed in S1 is likely inherited from slow decreases in thalamic firing rate and synchrony. Despite the degraded sensory responses, adaptation resulted in a shift in coding strategy that favors theoretical discrimination over detection across the observed timescales of adaptation. Overall, although multiple mechanisms contribute to rapid adaptation at distinct timescales, they support a unifying framework on the role of adaptation in sensory processing.

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Weeds are attractive models for basic and applied research due to their impacts on agricultural systems and capacity to swiftly adapt in response to anthropogenic selection pressures. Currently, a lack of genomic information precludes research to elucidate the genetic basis of rapid adaptation for important traits like herbicide resistance and stress tolerance and the effect of evolutionary mechanisms on wild populations. The International Weed Genomics Consortium is a collaborative group of scientists focused on developing genomic resources to impact research into sustainable, effective weed control methods and to provide insights about stress tolerance and adaptation to assist crop breeding.

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Agricultural insect pests (AIPs) are widely successful in adapting to natural and anthropogenic stressors, repeatedly overcoming population bottlenecks and acquiring resistance to intensive management practices. Although they have been largely overlooked in evolutionary studies, AIPs are ideal systems for understanding rapid adaptation under novel environmental conditions. Researchers have identified several genomic mechanisms that likely contribute to adaptive stress responses, including positive selection on de novo mutations, polygenic selection on standing allelic variation and phenotypic plasticity (e.g., hormesis). However, new theory suggests that stress itself may induce epigenetic modifications, which may confer heritable physiological changes (i.e., stress-resistant phenotypes). In this perspective, we discuss how environmental stress from agricultural management generates the epigenetic and genetic modifications that are associated with rapid adaptation in AIPs. We summarise existing evidence for stress-induced evolutionary processes in the context of insecticide resistance. Ultimately, we propose that studying AIPs offers new opportunities and resources for advancing our knowledge of stress-induced evolution.

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Copy number variation is a common contributor to phenotypic diversity, yet its involvement in ecological adaptation is not easily discerned. Instances of parallelly evolving populations of the same species in a similar environment marked by strong selective pressures present opportunities to study the role of copy number variants (CNVs) in adaptation. By identifying CNVs that repeatedly occur in multiple populations of the derived ecotype and are not (or are rarely) present in the populations of the ancestral ecotype, the association of such CNVs with adaptation to the novel environment can be inferred. We used this paradigm to identify CNVs associated with recurrent adaptation of the Mexican tetra (Astyanax mexicanus) to cave environment. Using a read-depth approach, we detected CNVs from previously re-sequenced genomes of 44 individuals belonging to two ancestral surfaces and three derived cave populations. We identified 102 genes and 292 genomic regions that repeatedly diverge in copy number between the two ecotypes and occupy 0.8% of the reference genome. Functional analysis revealed their association with processes previously recognized to be relevant for adaptation, such as vision, immunity, oxygen consumption, metabolism, and neural function and we propose that these variants have been selected for in the cave or surface waters. The majority of the ecotype-divergent CNVs are multiallelic and display copy number increases in cavefish compared to surface fish. Our findings suggest that multiallelic CNVs - including gene duplications - and divergence in copy number provide a fast route to produce novel phenotypes associated with adaptation to subterranean life.

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Fish hatcheries are widely used to enhance fisheries and supplement declining wild populations. However, substantial evidence suggests that hatchery fish are subject to differential selection pressures compared to their wild counterparts. Domestication selection, or adaptation to the hatchery environment, poses a risk to wild populations if traits specific to success in the hatchery environment have a genetic component and there is subsequent introgression between hatchery and wild fish. Few studies have investigated domestication selection in hatcheries on a genomic level, and even fewer have done so in parallel across multiple hatchery-wild population pairs. In this study, we used low-coverage whole-genome sequencing to investigate signals of domestication selection in three separate hatchery populations of Chinook salmon, Oncorhynchus tshawytscha, after approximately seven generations of divergence from their corresponding wild progenitor populations. We sequenced 192 individuals from populations across Southeast Alaska and estimated genotype likelihoods at over six million loci. We discovered a total of 14 outlier peaks displaying high genetic differentiation (F ST) between hatchery-wild pairs, although no peaks were shared across the three comparisons. Peaks were small (53 kb on average) and often displayed elevated absolute genetic divergence (D xy) and linkage disequilibrium, suggesting some level of domestication selection has occurred. Our study provides evidence that domestication selection can lead to genetic differences between hatchery and wild populations in only a few generations. Additionally, our data suggest that population-specific adaptation to hatchery environments likely occurs through different genetic pathways, even for populations with similar standing genetic variation. These results highlight the need to collect paired genotype-phenotype data to understand how domestication may be affecting fitness and to identify potential management practices that may mitigate genetic risks despite multiple pathways of domestication.

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The rapid adaptive evolution of microbes is driven by strong selection pressure acting on genetic variation. How adaptive genetic variation is generated within species and how such variation influences phenotypic trait expression is often not well understood though. We focused on the recent activity of transposable elements (TEs) using deep population genomics and transcriptomics analyses of a fungal plant pathogen with a highly active content of TEs in the genome. Zymoseptoria tritici causes one of the most damaging diseases on wheat, with recent adaptation to the host and environment being facilitated by TE-associated mutations. We obtained genomic and RNA-sequencing data from 146 isolates collected from a single wheat field. We established a genome-wide map of TE insertion polymorphisms in the population by analyzing recent TE insertions among individuals. We quantified the locus-specific transcription of individual TE copies and found considerable population variation at individual TE loci in the population. About 20% of all TE copies show transcription in the genome suggesting that genomic defenses such as repressive epigenetic marks and repeat-induced polymorphisms are at least partially ineffective at preventing the proliferation of TEs in the genome. A quarter of recent TE insertions are associated with expression variation of neighboring genes providing broad potential to influence trait expression. We indeed found that TE insertions are likely responsible for variation in virulence on the host and potentially diverse components of secondary metabolite production. Our large-scale transcriptomics study emphasizes how TE-derived polymorphisms segregate even in individual microbial populations and can broadly underpin trait variation in pathogens.IMPORTANCEPathogens can rapidly adapt to new hosts, antimicrobials, or changes in the environment. Adaptation arises often from mutations in the genome; however, how such variation is generated remains poorly understood. We investigated the most dynamic regions of the genome of Zymoseptoria tritici, a major fungal pathogen of wheat. We focused on the transcription of transposable elements. A large proportion of the transposable elements not only show signatures of potential activity but are also variable within a single population of the pathogen. We find that this variation in activity is likely influencing many important traits of the pathogen. Hence, our work provides insights into how a microbial species can adapt over the shortest time periods based on the activity of transposable elements.

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Experimental introductions of species have provided some of the most tractable examples of rapid phenotypic changes, which may reflect plasticity, the impact of stochastic processes, or the action of natural selection. Yet to date, very few studies have investigated the neutral and potentially adaptive genetic impacts of experimental introductions. We dissect the role of these processes in shaping the population differentiation of wall lizards in three Croatian islands (Susac, Pod Kopiste, and Pod Mrcaru), including the islet of Pod Mrcaru, where experimentally introduced lizards underwent rapid (~30 generations) phenotypic changes associated with a shift from an insectivorous to a plant-based diet. Using a genomic approach (~82,000 ddRAD loci), we confirmed a founder effect during introduction and very low neutral genetic differentiation between the introduced population and its source. However, genetic depletion did not prevent rapid population growth, as the introduced lizards exhibited population genetic signals of expansion and are known to have reached a high density. Our genome-scan analysis identified just a handful of loci showing large allelic shifts between ecologically divergent populations. This low overall signal of selection suggests that the extreme phenotypic differences observed among populations are determined by a small number of large-effect loci and/or that phenotypic plasticity plays a major role in phenotypic changes. Nonetheless, functional annotation of the outlier loci revealed some candidate genes relevant to diet-induced adaptation, in agreement with the hypothesis of directional selection. Our study provides important insights on the evolutionary potential of bottlenecked populations in response to new selective pressures on short ecological timescales.

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Alopecurus myosuroides (blackgrass) is a problematic weed of Western European winter wheat, and its success is largely due to widespread multiple-herbicide resistance. Previous analysis of F2 seed families derived from two distinct blackgrass populations exhibiting equivalent non-target site resistance (NTSR) phenotypes shows resistance is polygenic and evolves from standing genetic variation. Using a CIDER-seq pipeline, we show that herbicide-resistant (HR) and herbicide-sensitive (HS) F3 plants from these F2 seed families as well as the parent populations they were derived from carry extra-chromosomal circular DNA (eccDNA). We identify the similarities and differences in the coding structures within and between resistant and sensitive populations. Although the numbers and size of detected eccDNAs varied between the populations, comparisons between the HR and HS blackgrass populations identified shared and unique coding content, predicted genes, and functional protein domains. These include genes related to herbicide detoxification such as Cytochrome P450s, ATP-binding cassette transporters, and glutathione transferases including AmGSTF1. eccDNA content was mapped to the A. myosuroides reference genome, revealing genomic regions at the distal end of chromosome 5 and the near center of chromosomes 1 and 7 as regions with a high number of mapped eccDNA gene density. Mapping to 15 known herbicide-resistant QTL regions showed that the eccDNA coding sequences matched twelve, with four QTL matching HS coding sequences; only one region contained HR coding sequences. These findings establish that, like other pernicious weeds, blackgrass has eccDNAs that contain homologs of chromosomal genes, and these may contribute genetic heterogeneity and evolutionary innovation to rapidly adapt to abiotic stresses, including herbicide treatment.

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Cichlid fishes are textbook examples of explosive speciation and adaptive radiation, providing a great opportunity to understand how the genomic substrate yields extraordinary species diversity. Recently, we performed comparative genomic analyses of three Lake Victoria cichlids to reveal the genomic substrates underlying their rapid speciation and adaptation. We found that long divergent haplotypes derived from large-scale standing genetic variation, which originated before the adaptive radiation of Lake Victoria cichlids, may have contributed to their rapid diversification. In addition, the present study on genomic data from other East African cichlids suggested the reuse of alleles that may have originated in the ancestral lineages of Lake Tanganyika cichlids during cichlid evolution. Therefore, our results highlight that the primary factor that could drive repeated adaptive radiation across East African cichlids was allelic reuse from standing genetic variation to adapt to their own specific environment. In this report, we summarize the main results and discuss the evolutionary mechanisms of cichlids, based on our latest findings.

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Evidence has emerged that environmentally-induced epigenetic changes can have long-lasting effects on gene transcription across generations. These recent findings highlight the need to investigate the transgenerational impacts of pollutants to assess their long term effects on populations. In this study, we investigated the transgenerational effect of cadmium on zebrafish across 4 generations. A first whole methylome approach carried out on fish of the first two generations led us to focus our investigations on the estradiol receptor alpha gene (esr1). We observed a sex-dependent transgenerational inheritance of Cd-induced DNA methylation changes up to the last generation. These changes were associated with single nucleotide polymorphisms (SNPs) that were themselves at the origin of the creation or deletion of methylation sites. Thus, Cd-induced genetic selection gave rise to DNA methylation changes. We also analyzed the transcription level of various sections of esr1 as well as estrogen responsive genes. While Cd triggered transgenerational disorders, Cd-induced epigenetic changes in esr1 contributed to the rapid transgenerational adaptation of fish to Cd. Our results provide insight into the processes underpinning rapid adaptation and highlight the need to maintain genetic diversity within natural populations to bolster the resilience of species faced with the global environmental changes.

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Adaptation can occur at remarkably short timescales in natural populations, leading to drastic changes in phenotypes and genotype frequencies over a few generations only. The inference of demographic parameters can allow understanding how evolutionary forces interact and shape the genetic trajectories of populations during rapid adaptation. Here we propose a new Approximate Bayesian Computation (ABC) framework that couples a forward and individual-based model with temporal genetic data to disentangle genetic changes and demographic variations in a case of rapid adaptation. We test the accuracy of our inferential framework and evaluate the benefit of considering a dense versus sparse sampling. Theoretical investigations demonstrate high accuracy in both model and parameter estimations, even if a strong thinning is applied to time series data. Then, we apply our ABC inferential framework to empirical data describing the population genetic changes of the poplar rust pathogen following a major event of resistance overcoming. We successfully estimate key demographic and genetic parameters, including the proportion of resistant hosts deployed in the landscape and the level of standing genetic variation from which selection occurred. Inferred values are in accordance with our empirical knowledge of this biological system. This new inferential framework, which contrasts with coalescent-based ABC analyses, is promising for a better understanding of evolutionary trajectories of populations subjected to rapid adaptation.

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Eco-evolutionary interactions following ecosystem change provide critical insight into the ability of organisms to adapt to shifting resource landscapes. Here we explore evidence for the rapid parallel evolution of trout feeding morphology following eco-evolutionary interactions with zooplankton in alpine lakes stocked at different points in time in the Wind River Range (Wyoming, USA). In this system, trout predation has altered the zooplankton species community and driven a decrease in average zooplankton size. In some lakes that were stocked decades ago, we find shifts in gill raker traits consistent with the hypothesis that trout have rapidly adapted to exploit available smaller-bodied zooplankton more effectively. We explore this morphological response in multiple lake populations across two species of trout (cutthroat trout, Oncorhynchus clarkii, and golden trout Oncorhynchus aguabonita) and examine the impact of resource availability on morphological variation in gill raker number among lakes. Furthermore, we present genetic data to provide evidence that historically stocked cutthroat trout populations likely derive from multiple population sources, and incorporate variation from genomic relatedness in our exploration of environmental predictors of feeding morphology. These findings describe rapid adaptation and eco-evolutionary interactions in trout and document an evolutionary response to novel, contemporary ecosystem change.

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Contemporary anthropogenic changes in climate and landscape form a complex set of selective pressures acting on natural systems, yet, in many systems, we lack information about both whether and how organisms may adapt to these changes. In plants, research has focused on climate-induced changes in phenology and the resultant potential for disruption of plant-pollinator interactions, however, there remains a paucity of knowledge regarding how other pollinator-mediated traits may be involved in the adaptive response. Here, we use resurrection experiments to investigate the phenotypic basis of adaptation in a mixed-mating system plant, the common morning glory (Ipomoea purpurea). Specifically, we measure temporal and spatial changes in traits grouped into three categories relevant to plant-pollinator interactions - floral morphology, floral rewards, and floral phenology. We show a significant temporal increase in corolla size and shift to earlier flowering times, as well as a potential for increased investment in floral rewards, all of which are driven primarily by populations at more northern latitudes. Additionally, we find evidence for directional selection on floral morphology and phenology and evidence of balancing selection acting on anther-stigma distance. Overall, these results show an adaptive response in line with greater investment in pollinator attraction rather than self-pollination and fine-scale spatial differences in adaptive potential.

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Repeated herbicide applications in agricultural fields exert strong selection on weeds such as blackgrass (Alopecurus myosuroides), which is a major threat for temperate climate cereal crops. This inadvertent selection pressure provides an opportunity for investigating the underlying genetic mechanisms and evolutionary processes of rapid adaptation, which can occur both through mutations in the direct targets of herbicides and through changes in other, often metabolic, pathways, known as non-target-site resistance. How much target-site resistance (TSR) relies on de novo mutations vs. standing variation is important for developing strategies to manage herbicide resistance. We first generated a chromosome-level reference genome for A. myosuroides for population genomic studies of herbicide resistance and genome-wide diversity across Europe in this species. Next, through empirical data in the form of highly accurate long-read amplicons of alleles encoding acetyl-CoA carboxylase (ACCase) and acetolactate synthase (ALS) variants, we showed that most populations with resistance due to TSR mutations-23 out of 27 and six out of nine populations for ACCase and ALS, respectively-contained at least two TSR haplotypes, indicating that soft sweeps are the norm. Finally, through forward-in-time simulations, we inferred that TSR is likely to mainly result from standing genetic variation, with only a minor role for de novo mutations.

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The powdery mildew fungi (Erysiphaceae) are globally distributed plant pathogens with a range of more than 10,000 plant hosts. In this review, we discuss the long- and short-term evolution of these obligate biotrophic fungi and outline their diversity with respect to morphology, lifestyle, and host range. We highlight their remarkable ability to rapidly overcome plant immunity, evolve fungicide resistance, and broaden their host range, for example, through adaptation and hybridization. Recent advances in genomics and proteomics, particularly in cereal powdery mildews (genus Blumeria), provided first insights into mechanisms of genomic adaptation in these fungi. Transposable elements play key roles in shaping their genomes, where even close relatives exhibit diversified patterns of recent and ongoing transposon activity. These transposons are ubiquitously distributed in the powdery mildew genomes, resulting in a highly adaptive genome architecture lacking obvious regions of conserved gene space. Transposons can also be neofunctionalized to encode novel virulence factors, particularly candidate secreted effector proteins, which may undermine the plant immune system. In cereals like barley and wheat, some of these effectors are recognized by plant immune receptors encoded by resistance genes with numerous allelic variants. These effectors determine incompatibility ("avirulence") and evolve rapidly through sequence diversification and copy number variation. Altogether, powdery mildew fungi possess plastic genomes that enable their fast evolutionary adaptation towards overcoming plant immunity, host barriers, and chemical stress such as fungicides, foreshadowing future outbreaks, host range shifts and expansions as well as potential pandemics by these pathogens.

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Ecologists and evolutionary biologists are increasingly cognizant of rapid adaptation in wild populations. Rapid adaptation to anthropogenic environmental change is critical for maintaining biodiversity and ecosystems services into the future. Anthropogenic salinization of freshwater ecosystems is quickly emerging as a primary threat, which is well documented in the northern temperate ecoregion. Specifically, many northern temperate lakes have undergone extensive salinization because of urbanization and the associated increase in impervious surfaces causing runoff, and the extensive use of road deicing salts (e.g., NaCl). It remains unclear whether increasing salinization will lead to extirpation of species from these systems. Using a "resurrection genomics" approach, we investigated whether the keystone aquatic herbivore, Daphnia pulicaria, has evolved increased salinity tolerance in a severely salinized lake located in Minnesota, USA. Whole-genome resequencing of 54 Daphnia clones from the lake and hatched from resting eggs that represent a 25-y temporal contrast demonstrates that many regions of the genome containing genes related to osmoregulation are under selection in the study population. Tolerance assays of clones revealed that the most recent clones are more tolerant to salinity than older clones; this pattern is concomitant with the temporal pattern of stabilizing salinity in this lake. Together, our results demonstrate that keystone species such as Daphnia can rapidly adapt to increasing freshwater salinization. Further, our results indicate that rapid adaptation to salinity may allow lake Daphnia populations to persist in the face of anthropogenic salinization maintaining the food webs and ecosystem services they support despite global environmental change.

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Urbanization drastically transforms landscapes, resulting in fragmentation, degradation, and the loss of local biodiversity. Yet, urban environments also offer opportunities to observe rapid evolutionary change in wild populations that survive and even thrive in these novel habitats. In many ways, cities represent replicated "natural experiments" in which geographically separated populations adaptively respond to similar selection pressures over rapid evolutionary timescales. Little is known, however, about the genetic basis of adaptive phenotypic differentiation in urban populations nor the extent to which phenotypic parallelism is reflected at the genomic level with signatures of parallel selection. Here, we analyzed the genomic underpinnings of parallel urban-associated phenotypic change in Anolis cristatellus, a small-bodied neotropical lizard found abundantly in both urbanized and forested environments. We show that phenotypic parallelism in response to parallel urban environmental change is underlain by genomic parallelism and identify candidate loci across the Anolis genome associated with this adaptive morphological divergence. Our findings point to polygenic selection on standing genetic variation as a key process to effectuate rapid morphological adaptation. Identified candidate loci represent several functions associated with skeletomuscular development, morphology, and human disease. Taken together, these results shed light on the genomic basis of complex morphological adaptations, provide insight into the role of contingency and determinism in adaptation to novel environments, and underscore the value of urban environments to address fundamental evolutionary questions.

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The growth rate hypothesis (GRH) posits that the relative body phosphorus content of an organism is positively related to somatic growth rate, as protein synthesis, which is necessary for growth, requires P-rich rRNA. This hypothesis has strong support at the interspecific level. Here, we explore the use of the GRH to predict microevolutionary responses in consumer body stoichiometry. For this, we subjected populations of the rotifer Brachionus calyciflorus to selection for fast population growth rate (PGR) in P-rich (HPF) and P-poor (LPF) food environments. With common garden transplant experiments, we demonstrate that in HP populations evolution toward increased PGR was concomitant with an increase in relative phosphorus content. In contrast, LP populations evolved higher PGR without an increase in relative phosphorus content. We conclude that the GRH has the potential to predict microevolutionary change, but that its application is contingent on the environmental context. Our results highlight the potential of cryptic evolution in determining the performance response of populations to elemental limitation of their food resources.

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Despite still being a matter of debate, there is growing evidence that pollutant-induced epigenetic changes can be propagated across generations. Whereas such modifications could have long-lasting effects on organisms and even on population, environmentally relevant data from long-term exposure combined with follow-up through multiple generations remain scarce for non-mammalian species. We performed a transgenerational experiment comprising four successive generations of zebrafish. Only fish from the first generation were exposed to an environmentally realistic concentration of cadmium (Cd). Using a whole methylome analysis, we first identified the DNA regions that were differentially methylated in response to Cd exposure and common to fish of the first two generations. Among them, we then focused our investigations on the exon 3 (ex3) of the cep19 gene. We indeed recorded transgenerational growth disorders in Cd-exposed fish, and a mutation in this exon is known to cause morbid obesity in mammals. Its methylation level was thus determined in zebrafish from all the four generations by means of a targeted and base resolution method. We observed a transgenerational inheritance of Cd-induced DNA methylation changes up to the fourth generation. However, these changes were closely associated with genetic variations, mainly a single nucleotide polymorphism. This single nucleotide polymorphism was itself at the origin of the creation or deletion of a methylation site and deeply impacted the methylation level of neighboring methylation sites. Cd-induced epigenetic changes were associated with different mRNA transcripts and an improved condition of Cd fish. Our results emphasize a tight relationship between genetic and epigenetic mechanisms and suggest that their interplay and pre-existing diversity can allow rapid adaptation to anthropogenic environmental changes.