Evolution Letters

Populations often persist in novel environments despite predictions that adaptive capacity to such conditions should be limited by a lack of genetic variation. A leading hypothesis is that genetic variation for adapting to novel environments is maintained but remains hidden under native conditions. However, direct evidence for the mechanisms that maintain this adaptive potential in natural populations is scarce. Here, we integrate data from four large-scale field experiments to test whether variation in selection across life history and environments, together with genetic architecture, maintains genetic variation important for adapting to novel environments. Using a quantitative genetic breeding design, we generated families of the Sicilian daisy, Senecio chrysanthemifolius (Asteraceae), and planted seeds and cuttings across native and novel elevations on Mount Etna. We tracked fitness across elevations, life stages, seasons and generations. Genotypes with higher survival and flowering success at the novel elevation increased adaptive potential, but were only weakly selected against in the native environment where they had slightly lower fitness at a later life-history stage. A negative genetic correlation in seedling survival across seasons indicated that different genotypes were favoured across temporal variation in native environments. Crosses between genotypes with low and high fitness in the novel environment revealed that genotypes that increased adaptive potential had heritable effects on plasticity and fitness across generations, but were recessive and therefore largely hidden in heterozygotes. Together, these results provide rare field-based evidence that weak selection in native environments, temporal variation in selection and dominance effects act together to maintain cryptic adaptive potential in natural populations.

Transgenerational plasticity (TGP)- when parental environments influence offspring phenotypes - is ubiquitous across taxonomic groups and can have benefits for offspring beyond what is possible with developmental plasticity, particularly when selective pressures are high early in life. However, patterns of TGP vary widely across populations and species, and the evolutionary processes shaping this variation remain poorly understood. Here, we tested whether repeated evolutionary transitions result in parallel or population-specific evolutionary divergence in TGP relative to ancestral conditions. We examined sperm-mediated paternal effects across two ancestral marine and three derived freshwater populations of threespined stickleback fish (Gasterosteus aculeatus). We exposed fathers to dragonfly larvae (endemic to freshwater) or sculpin (endemic to all populations) predators and measured both paternal response to predators as well as antipredator behavior and growth in larval offspring. Fathers behaviorally responded to the presence of sculpin predators, but not dragonfly larvae. However, we found strong paternal effects in response to both predators in all populations. Further, the magnitude of TGP did not differ between marine and freshwater populations, suggesting that TGP does not become genetically accommodated as marine populations move into freshwater habitats. We found some evidence consistent with parallelism in both within and trans-generational plasticity: 1) personal exposure of larval stickleback to dragonfly larvae elicited strong antipredator responses in freshwater populations that were absent in marine populations, and 2) paternal predation exposure consistently increased offspring growth in marine populations while slowing growth in freshwater populations. In contrast, paternal effects altered offspring behavior in population-specific ways, with strong sex-specific effects of paternal exposure emerging in response to endemic predators. Adaptive evolution is a two-step process, in which heritable genotypic and phenotypic variation must first be present and then selected on. Therefore, high population-level variation in TGP suggests the capacity for rapid evolution of parental effects, while signatures of parallelism and sex-specific patterns suggest that TGP may evolve in targeted ways in response to ecological stressors.

Inbreeding depression is a critical driver of extinction risk in fragmented populations, yet its magnitude in the wild has historically been estimated using sparse pedigrees or low-resolution molecular markers. The transition to genomic metrics of inbreeding offers unprecedented precision in quantifying realized homozygosity and its fitness costs. We conducted a systematic review and multi-level meta-analysis of 91 effect sizes from 20 wild vertebrate populations to provide a global benchmark for genomic inbreeding depression. Our results confirm a pervasive and significant negative relationship between fitness and genomic inbreeding. Males exhibited significantly stronger inbreeding depression than females. Fitness costs were consistent across life stages (developmental, adult and lifetime) and across types of fitness traits (survival vs. reproduction). We found no significant association between the magnitude of inbreeding depression and IUCN conservation status or historical isolation (discretely measured as "isolated" or "non-isolated"). As we enter a genomics era that will provide realised estimates of inbreeding, future studies can be added to this meta-analysis to provide a more comprehensive view of inbreeding depression and potentially identify patterns pertinent to evolutionary biology and conservation science.

The potential for environmental change to compound the detrimental effects of inbreeding depression in small and isolated populations is a significant concern in conservation biology. Previous evidence syntheses suggested that environmental stress exacerbates inbreeding depression, but were based on limited data. Here, we comprehensively test the relationship between inbreeding depression and environmental stress in natural populations using Bayesian mixed-effects meta-analysis on a large, high-quality data set of 2127 inbreeding depression effect sizes from animals and plants. Our results show that inbreeding depression is significantly higher in benign than in stressful environments. Analyses of both inbreeding depression and stress-induced changes in genetic load supported a unimodal (humped) relationship between the costs of inbreeding and stress intensity, with a peak at intermediate stress. At the highest levels of stress there was, on average, a significantly greater inbreeding load in benign than in stressful environments. We suggest that the lower cost of inbreeding associated with extreme stress results from constraints on the expression of inbreeding depression as fitness and phenotypes decline towards zero. Our findings help to resolve long-standing uncertainty around how inbreeding and environmental change interact, revealing that inbreeding responses vary non-linearly with environmental stress intensity, but showing that stress does not generally amplify inbreeding depression. As such, they will inform both the management of populations of conservation concern and predictions of species responses to global environmental change.

Does the distribution of fitness effects of new mutations vary across the genome? Under the classical Fisher Geometric Model (FGM) we might not expect it to. In FGM, phenotypic traits are envisioned as dimensions of a landscape, with fitness determined by position in the landscape, i.e., the particular combination of traits of an individual. New mutations are represented by vectors that move from an ancestral to a new phenotype. In classical FGM these vectors affect all trait dimensions simultaneously (universal pleiotropy). However, introducing partial and modular pleiotropy into an FGM framework leads to an expectation that parameters of the DFE will vary with mutational pleiotropy-the number of traits affected by individual mutations. Here we address this prediction by investigating whether traits related to mutational pleiotropy, expression level and network connectivity, affect the parameters of the DFE using whole genome data from A. thaliana and C. grandiflora, two closely related Brassica species that vary significantly in their demography and mating system, and therefore, in effective population size and the effects of linked selection. Results were similar across both species. We found that expression level and network connectivity were predictive of the parameters of the deleterious DFE, even once co-correlations among genome biology traits were accounted for. Our results suggest that, across the genome, molecular evolutio(high mutational pleiotropy). nary patterns agree with the predictions of FGM, albeit relaxing the assumption of universal pleiotropy, and that variation in mutational pleiotropy among genes is sufficient to have detectible effects on the DFE. Significance statementHow do the effects of new mutations vary across the genome? If mutations in some genes affect many traits (high mutational pleiotropy), we hypothesise they will be more strongly deleterious, with lower variance in their selective effects. We test this by investigating the distribution of effects of new mutations across genes that vary in features that are related to mutational pleiotropy: expression level, gene network connectivity, and number of associated GO terms. The mean strength and coefficient of variation of selection of new mutations varied across genes with different features in the manner expected by our hypothesis. This demonstrates that important parameters of molecular evolution can vary across the genome with genome architecture.

Hosts defend themselves against parasites through resistance (reducing parasite burden) and tolerance (reducing the fitness cost of infection without affecting parasites). This distinction has important evolutionary implications: resistance is predicted to maintain polymorphism while tolerance tends to fix, and only resistance is expected to provoke parasite counter-adaptation. The reaction-norm framework, which infers tolerance from the slope of host fitness regressed on parasite burden, assumes that a shallow slope reflects parasite-independent host protection. We test this assumption using a within-host model in two variants: microparasites (Model 1, with within-host replication) and macroparasites (Model 2, without). Sublethal immunity impairs the host-exploitation rate of the parasite, reducing both growth and per-parasite virulence without killing them. We show that this generates systematic slope differences among host genotypes that the framework interprets as variation in tolerance. Furthermore, the ranking of slopes across genotypes reverses between linear and sigmoidal damage functions: under linear damage, the strongest immune responder appears most tolerant; under sigmoidal damage, the weakest responder does. Decomposition of the damage reduction shows that virulence reduction accounts for the majority of the effect across both model variants. Thus, the reaction-norm slope cannot determine whether host fitness is maintained by parasite-independent tissue protection or by sublethal impairment of parasites.

Gene regulatory divergence has emerged as a key feature in speciation, influencing gene expression differences that accumulate between diverging populations. Transcriptional regulation, mediated by cis- and trans-acting factors, modulates diverse developmental processes and is responsible for distinct species-specific gene expression profiles. Within interspecies hybrid individuals, negative interactions between divergent cis- and trans-acting factors can lead to gene misregulation and hybrid dysfunction at the organismal level. Such gene regulatory mismatch might disproportionately impact sex-biased and tissue-biased gene regulatory networks due to their unique selective pressures. To address these issues, we investigated the role of regulatory divergence in asymmetric hybrid incompatibility between sister species of Caenorhabditis nematodes (C. remanei, C. latens) by analyzing gene expression of reciprocal hybrids for each sex and key tissue types. Despite severe hybrid male sterility, hybrid males showed less misexpression of sex-biased genes than hybrid females, suggesting that the organismal phenotypic outputs of male-biased gene regulatory networks are more vulnerable to disruption than female-biased genetic networks. Additionally, we found more genes associated with cis- than trans-regulatory divergence, supporting the notion of a disproportionate role for cis-regulatory divergence between species. Moreover, we document extensive cis-trans compensatory X-linked regulatory divergence specifically from male transcriptomes, indicating distinct molecular evolutionary outcomes of stabilizing selection on regulatory controls in males and females. These insights derived from asymmetric hybrid misexpression expand our understanding of the evolution of sex-biased gene regulation in the face of stabilizing selection and identify candidate genes contributing to Caenorhabditis post-zygotic reproductive isolation.

Genetic interventions to modify wild population densities are typically framed around pest suppression, with parallel approaches for boosting beneficial or endangered populations remaining largely undeveloped. Imposing a sustained but non-eliminative genetic load could in principle address both objectives, but existing designs rely on genes with intermediate fitness effects whose loads are difficult to predict under field conditions. Here we describe engineered balanced lethal systems, in which CRISPR-based gene drive establishes two complementing recessive-lethal alleles at a single locus, producing a sustained 50% load through Mendelian segregation. Modelling shows these systems spread from small releases, and that the resulting population-level consequences depend on density regulation and on the timing of lethality: the same 50% load can suppress pests, boost populations of beneficial or endangered species, dampen boom-bust cycles, or raise effective population size. Additional systems at independent loci scale the effect in stepwise increments, and a split-drive variant localises it geographically. These results demonstrate that gene drives imposing genetic load can be expanded beyond elimination, to support and preserve beneficial and endangered populations.

Co-occurring species often face similar selective environments, although adaptive responses to these environments are generally assumed to be species-specific, particularly in complex landscapes where selective pressures are likely to be multi-dimensional. We test this assumption by contrasting genotype-environment associations (GEAs) among a range of co-occurring but unrelated plants with different life histories from an isolated, mountainous national park in south-eastern Australia. Analyses were performed using single nucleotide polymorphism (SNP) loci derived from reduced genome representation sequencing to investigate genomic associations with spatial and environmental drivers across unrelated plant species within the same heterogeneous landscape. Several species showed GEAs that aligned with similar environmental gradients, particularly edaphic features, suggesting that similar selective pressures can shape genomic responses across taxa. Other species exhibited distinct spatial and environmental associations, highlighting idiosyncratic outcomes. Notably, GEAs were detected at fine spatial scales despite generally low levels of genome-wide divergence, suggesting adaptive variants can persist in the face of gene flow under strong selective pressure. This study highlights how community-level genomic diversity is shaped by common environmental processes, with implications for biodiversity management in rapidly changing environments, where diverse ecosystem-level responses to selection may underpin resilience.

Hybridization, the interbreeding between species or genetically distinct populations, can lead to deleterious fitness consequences, but simultaneously it can boost adaptive potential by increasing genetic variation, especially in novel environments. However, how incompatibilities and beneficial genetic combinations interplay across generations remains poorly understood. Here, we tracked how two fitness proxies, the absolute number of adult offspring and the proportion of eggs that reached adulthood, evolve in parental and hybrid populations at three different time points over 50 generations, in both novel and ancestral environments. To test this, we used two geographically distinct populations with low divergence (Dxy=0.002) of the two-spotted spider mite (Tetranychus urticae). Across the first three generations, hybrids showed significantly lower fitness than parental populations in the ancestral environment, indicating incompatibilities between the parental genomes. In contrast, hybrid and parental fitnesses were similar in the novel environment, indicating that the impact of incompatibilities was minor compared to the selection imposed by the novel environment. However, after 50 generations, hybrids displayed similar fitness relative to parental populations in all environments, suggesting resolution of the incompatibilities. Furthermore, around generation 45, hybrids temporarily outperformed parental populations in a novel environment, suggesting a transient window of higher adaptive potential, before fitness stabilized again by generation 50. In conclusion, we show that hybrid populations of T. urticae can swiftly purge incompatibilities when genetic divergence is low. These findings suggest that the dynamics of incompatibility resolution and adaptive potential of novel haplotypes play out over a long time frame, highlighting the importance of tracking hybrid fitness past the first few generations.

The between sex genetic correlation for traits has long been hypothesized as a constraint to the evolution of sexual dimorphism. Both empirical and theoretical work has suggested that this constraint is influenced by genotype-sex-environment interactions. We examine genotype-sex-environment interactions in both sexually exaggerated and non-exaggerated legs of Drosophila prolongata, to examine the role of organismal condition on evolvability of an extreme trait. We employed a nested full-sib half-sib crossing design, providing food either ad libitum, or restricting food during larval growth, to each brood. When provided food ad libitum, inter-sex genetic correlations between traits is high and positive, whereas under food restriction this correlation substantially weakens, with a modest negative sign. Similarly, comparisons of the G matrix across sexes becomes less associated under food restriction. We discuss these results in the context of the growing appreciation of the factors that facilitate sex-specific evolutionary change.

Understanding the role of sexual selection in shaping evolutionary trajectories is a key goal of biology, and thus developing a genomic measure of sexual selection strength is desirable. In systems with ZW sex determination, the ratio of nucleotide diversity ({pi}) on the male-biased Z chromosome to that on the autosomes (the Z:A ratio) is expected to decline as male effective population size decreases under strong sexual selection, offering one such measure. However, non-equilibrium processes other than sexual selection (e.g., hybridization, changes in population size) can influence levels of Z-linked diversity relative to the rest of the genome, complicating interpretation of this metric and necessitating a systematic evaluation of how Z:A ratios vary across known demographic and selective circumstances. We leveraged longitudinal sampling over a [~]25-year period in Manacus manakin populations in western Panama, spanning a mainland transect (including M. candei, M. vitellinus, and their hybrid zone) and insular populations of the Bocas del Toro Archipelago. On the mainland, Z:A ratios were temporally stable within populations, but varied across populations: (1) Z:A ratios were lower in M. vitellinus than M. candei, likely due to stronger sexual selection in the former; and (2) Z:A ratios increased at the hybrid zone center, likely due to fast-Z effects in parentals inflating Z:A ratios in recent hybrids. Island populations exhibited significantly lower Z:A ratios than mainland populations, consistent with theoretical expectations of Z:A reductions following population contractions as the islands became isolated. Insular Z:A ratios increased with proximity to other landmasses, suggesting gene flow mitigates these effects in this system. While the Z:A ratio behaved predictably in relation to known non-equilibrium processes, our results demonstrate the potentially strong effects of demographic history and admixture on Z-linked diversity, which should be considered in studies aiming to use the Z:A ratio as a measure of sexual selection.

Rapid adaptation in complex environments depends not only on the amount of genetic variation, but also on patterns of covariation among traits targeted by selection. Anthropogenic stressors create rapidly changing and multifaceted environments and provide powerful systems in which to investigate the potential for adaptation to multiple coinciding stressors. We investigate the combined effects of heat and chemical stress on survival in the black scavenger fly, Sepsis neocynipsea, and determine the genetic basis for resistance. In a fully factorial experiment, we expose isofemale lines to combinations of heat stress and ivermectin, a veterinary antiparasitic to which these flies are naturally exposed in agricultural landscapes. Using a Bayesian quantitative genetic approach, we estimate broad-sense genetic variation and cross-environmental genetic correlations. First, we show that these two stressors have synergistic effects on survival, with heat stress exacerbating the lethal effects of ivermectin. Second, we find that the largest component of genetic variation is the response to heat and ivermectin in combination (genotype-by-environment-by-environment; GxExE). Third, cross-environmental genetic correlations are weak, implying that relative genetic performance is dependent on the specific combination of stressors. Together, these results suggest that incorporating GxExE is essential for understanding adaptive potential in multi-stressor environments.

Environmental predation is a major driver of bacterial evolution and may indirectly influence virulence through coincidental selection. However, how sustained versus fluctuating predator pressure shapes long-term evolutionary trajectories remains poorly understood. Here, we used experimental evolution to investigate the genetic and phenotypic responses of Pseudomonas aeruginosa to continuous, absent, or fluctuating exposure to the protozoan predator Tetrahymena thermophila over 180 days. Whole-population and isolate-level shotgun metagenomic sequencing revealed fewer mutations over time but increasing frequencies of surviving mutations, consistent with selection, extensive gene-level parallel evolution, and signatures of both positive and purifying selection. Recurrently mutated genes encompassed diverse functional pathways, reflecting both shared and treatment-specific adaptive responses. Despite this parallelism, historical contingency was evident, with starting conditions influencing subsequent evolutionary trajectories. We also observed the emergence of hypermutator lineages, which are frequently recovered from chronic lung infections, suggesting that repeatedly evolving elevated mutation rates may represent a common adaptive strategy of P. aeruginosa across environmental and host-associated settings. Fluctuating predation repeatedly reshaped the adaptive landscape, leading to greater temporal turnover of mutations and a higher accumulation of mutations that ultimately reached fixation than in constant environments. Phenotypic assays revealed widespread divergence in fitness, motility, biofilm formation, siderophore production, protease activity, hemolysis, and cell size, whereas virulence in an invertebrate host model varied among treatments but did not differ significantly. Together, these findings demonstrate that variation in predator-mediated selection reshapes the dynamics and genetic targets of bacterial adaptation, highlighting the roles of ecological context, historical contingency, and hypermutability in driving the evolutionary trajectories of opportunistic pathogens. Significance StatementEnvironmental predators are drivers of bacterial evolution, yet their effects on adaptation remain poorly understood. We used experimental evolution to show that constant and fluctuating protozoan predation produce evolutionary trajectories in Pseudomonas aeruginosa, altering tempo, predictability, and targets of adaptation. Adaptation to predator-present or predator-absent environments shaped evolutionary trajectories, demonstrating importance of historical contingency. Fluctuating predation promoted turnover of mutations as populations adapted to selective pressures. We also observed repeated emergence of hypermutator lineages, a hallmark of chronic infections, suggesting that elevated mutation rates represent a favored adaptive strategy across environmental and host-associated settings. These findings provide insight into the environmental origins of genetic changes commonly associated with opportunistic pathogens, while showing that these changes do not necessarily increase virulence.

Genetic drift and natural selection jointly shape how populations evolve during range expansion, yet their joint influence on fitness at expanding range margins is rarely examined. Serial founder events during range expansion may amplify genetic drift and result in the accumulation (or greater expression) of deleterious mutations at range margins, termed expansion load. Conversely, natural selection should lead to local adaptation during expansion provided that populations harbor adequate genetic variation. We used a manipulative transplant experiment, genome-wide SNP data, and demographic surveys of the invasive plant, commontansy (Tanacetum vulgare), to evaluate evidence for expansion load and local adaptation during ca. 150 years of invasion in Minnesota, U.S.A. The common garden occurred near the southern range margin and included 16 populations that span (1) a chronosequence of invasion from northeastern MN (invasion core) to southern and western range margins and (2) environmental gradients in temperature and precipitation. We also manipulated temperature and precipitation to test whether environmental stress amplified the expression of expansion load or revealed population differentiation in climate adaptation. Population fitness declined strongly with distance from the invasion core, consistent with the accumulation of expansion load. This finding was corroborated by analyses of 173 populations that showed an increase in homozygosity (F) and a decrease in population size from the invasion core to range margins. We did not find any evidence of local adaptation; a strong positive relationship between population mean fitness and environmental distance was indicative of maladaptation. While the elevated temperature manipulation reduced fitness, it did not amplify the expression of expansion load. Taken together, our results are consistent with the hypothesis that serial population bottlenecks and strong genetic drift led to expansion load and reduced fitness at range margins. Teaser TextSpecies geographic ranges are dynamic over geologic time scales but may also shift rapidly in response to climate change and for invasive species. While range shifts are often viewed only through an ecological lens, the extent and pace of range expansion may be significantly modulated by evolutionary processes. We disentangled the influence of genetic drift and natural selection on population fitness across an invasion chronosequence (spanning ca. 150 years) for the herbaceous plant common tansy (Tanacetum vulgare). Our synthesis of analyses of a field transplant experiment, genome-wide SNP data, and demographic surveys provided evidence consistent with the accumulation of expansion load at leading range edges. While theory often predicts that local adaptation should occur readily in response to novel environments, our results were consistent with local maladaptation. Our findings emphasize the importance of stochastic processes in shaping the geographic distribution of species and their capacity to shift with changing environments.

Climate change can threaten population viability by disrupting sex ratios in species whose sex is influenced by temperature. While species with sex chromosomes were historically considered immune, in some species, temperatures can override genetic sex determination via sex reversal, leaving them vulnerable to climate-driven sex ratio shifts. The Tasmanian spotted snow skink (Carinacincus ocellatus), a viviparous reptile with an XX/XY system, provides a compelling case study. While laboratory studies demonstrated that extreme thermal conditions induce female-to-male sex reversal (XX males), its occurrence in the wild remains unexplored, limiting our understanding of actual climate impacts. Integrating 23 years of phenotypic and genetic sexing data across two climatically distinct populations, we provide the first evidence of sex reversal in a wild viviparous reptile. XX reversal occurred in both populations, affecting up to 23.5% of XX births in the warmer population, and was associated with colder minimum daily temperatures. Despite high birth rates in some years, sex-reversed adults were rare. We also identified putative XY females, suggesting bidirectional sex reversal and reinforcing the extreme plasticity of reptilian sex determination. Ultimately, sex reversal could act as an evolutionary trap, potentially compromising population viability as climate instability increases.

Long-term persistence of managed species will depend, in part, on whether the species harbors the physiological or genetic potential to adjust to warming temperatures, and whether relevant genetic variation is modified by management practices. The critically endangered Delta Smelt (Hypomesus transpacificus) is intensively managed, but little is known about the presence of genetic variation for resistance to elevated temperature, which will be important to maintain for their persistence in a rapidly warming future. Using a pedigree and whole genome sequencing data, we characterized the genetic variation and genomic architecture for CTMax (as a metric of upper thermal tolerance) across control and elevated rearing temperatures, alongside covarying traits (body size, degree of hatchery ancestry). Warmer rearing temperatures increased CTMax through acclimation but also resulted in reduced additive genetic variation for the trait, which could constrain adaptation under thermal stress. We found that larger fish had reduced CTMax, although this effect was diminished at elevated temperatures. We observed modest heritability for CTMax at rearing temperatures of 15{degrees}C and 18{degrees}C (0.26 and 0.16, respectively), but only a limited number of loci were identified that had consistent effects on CTMax across rearing temperatures. Instead, the genomic basis of thermal tolerance was highly dependent on rearing temperature (many loci detected with a GxE effect). The influence of domestication selection was indicated by changes in allele frequency, and divergence in upper thermal tolerance and plasticity, between low and high hatchery ancestry groups. Minimal overlap between loci associated with domestication and CTMax suggests that these traits possess separate genetic underpinnings. Knowledge of genetic variation supporting ecologically relevant physiological variation may be useful for refuge management and may inform supplementation in an ever-warming environment.

Herbicide resistance is among the clearest examples of rapid adaptation to intense anthropogenic selection. Yet, how the evolutionary origins and genetic architecture of resistance shapes its tempo and mode of evolution remain incompletely resolved. Here, we address these questions in Alopecurus myosuroides (blackgrass), Europe's most widespread and economically damaging herbicide-resistant weed. We present the first genome-wide analysis of herbicide resistance in natural blackgrass populations, uniquely combining historical and contemporary populations collected before and after the onset of intensive herbicide use. This temporal framework provides novel empirical access to pre-selection genetic variation, enabling reconstruction of the tempo and mode of both target-site (TSR) and non-target-site resistance (NTSR) evolution across space and time. TSR mutations were not found in pre-herbicide populations and evolved recently through repeated, largely independent origins across Europe. NTSR, in contrast, has a polygenic architecture and is associated with a cluster of glutathione S-transferases (GSTs) with signatures of copy number variation, and broader stress-response genes. Most NTSR-associated alleles were already segregating in historical populations, consistent with rapid adaptation from standing genetic variation. Moreover, resistance-associated loci show signatures consistent with positive selection predating herbicide use, suggesting these stress and detoxification pathways were historically maintained by prior ecological selection and subsequently recruited under herbicide pressure. Together, these findings demonstrate that herbicide resistance encompasses contrasting genetic routes, with polygenic NTSR evolving largely through selection on standing variation, offering broader insights into the evolutionary dynamics of rapid polygenic adaptation under novel anthropogenic selection.

Dominance is a widespread feature of genetic variants which affects life-history traits and fitness. Although dominance is generally thought to be an intrinsic property of genetic variants, it can sometimes evolve, as in the classic case of melanism in the peppered moth. The broader question of how likely dominance is to evolve is, however, controversial, because conditions favouring dominance evolution are often restrictive. Here, we revisit Haldanes classic hypothesis that dominance might evolve during the spread of beneficial mutations to fixation (i.e., during selective sweeps). We first confirm results of earlier models that sweeps of unconditionally beneficial mutations generate little potential for dominance to evolve, even in cases where modifier alleles segregate prior to selective sweeps. However, when sweeping beneficial alleles trade off between different environments -- which we explore with the illustrative case of sexually antagonistic selection -- the scope for dominance evolution expands. This occurs because modifier alleles can alter dominance separately in each environment, increasing the mean fitness of heterozygotes, prolonging the sojourn time of the sweep, and generating more heterozygosity upon which the modifier can act. In extreme cases, beneficial mutations that were initially destined for fixation can undergo a "dominance reversal" as a result of dominance evolution, converting them to balanced polymorphisms. We quantify how regularly dominance reversals of sweeping sexually antagonistic alleles can be expected to evolve. Overall, our results highlight conditions that allow the dominance of beneficial mutations to evolve, which we discuss in light of data on the frequency of selective sweeps, standing genetic variation for modifiers, and plasticity of modifier effects.

How broad phenotypic variation is maintained in natural populations in the face of selection is a central question in evolutionary biology. We address this question in the water strider Microvelia longipes, where males exhibit striking variation in rear leg length used in male-male contests for dominance. Using reaction norm experiments on inbred lines, we demonstrate that phenotypic plasticity contributes to expanding phenotypic variation, but requires high genetic variation to generate the broad range of trait expression observed in natural populations. Experimental evolution favouring trait exaggeration revealed that directional sexual selection not only fails to erode variation of male rear leg length, but rather amplifies it beyond the natural distribution. Additionally, male-limited selection in favour of dominance generated substantial fecundity costs in females, underscoring the role of sexual conflict driven by females in constraining exaggerated secondary sexual traits in males. Our findings show that sexually antagonistic selection and directional sexual selection jointly generate high genetic variation, which phenotypic plasticity inflates into broad phenotypic distribution of male weapon size. This provides an empirical explanation for the high variability of male exaggerated weapons in nature.