Evolution Letters

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.

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.

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.

A long-standing question in evolutionary biology is: Under what circumstances can speciation occur despite hybridisation or because of hybridisation? Some models of hybrid incompatibilities predict that speciation can occur even in the presence of gene flow and strong selection against hybrids, an outcome also influenced by genetic contributions from parental species and genetic architecture. On the other hand, empirical work has shown that heterosis can counteract the effect of incompatibilities, hindering the speciation process. Theoretical models that simultaneously consider the positive and negative impacts of hybridisation on fitness remain scarce, raising questions about the effects of hybrid incompatibilities in the presence of heterosis. To address this question, we study how (Bateson)-Dobzhansky-Muller incompatibilities (BDMIs) interact with overdominant mutations in a two-locus population genetics model of an isolated hybrid population. We find that the strength of overdominance relative to incompatibilities determines the long-term genetic composition of the hybrid population. We show that high recombination exposes incompatibilities to selection and reduces the frequency of derived alleles in the hybrid population, limiting the strength of BDMIs that can be maintained by the balance with overdominance. We also show how neutral variation is affected by the strength of selection and the recombination rate between incompatible loci, generating patterns that include an increase in local variation resembling associative overdominance, or a reduction resembling background selection. Such variation of neutral variation, particularly at intermediate distances from BDMI loci, can generate peaks or troughs of diversity that are explained by the recombination rate between BDMI loci, and initial proportions of admixture between parental populations. Our work demonstrates how the genomic conflict caused by the interplay of overdominance and hybrid incompatibilities, recombination, and parental contributions, shape the genome of an isolated hybrid population.

Sexually selected traits often impose fitness costs on their bearers. Yet, the relative costs and benefits of conspicuous traits can vary through space and time, driving variation in selection acting on those traits. For insects, an important but overlooked source of such variation is seasonal shifts in the local abundance of migratory insectivorous birds. Smoky rubyspot damselflies (Hetaerina titia) exhibit a marked seasonal polyphenism in wing pigmentation throughout much of North America, with individuals emerging in the summer exhibiting conspicuous dark wings. Here, we test the hypothesis that this variation is an adaptive response to seasonal and geographical variation in predation risk. First, we find evidence for strong constraints acting on wing phenotypes outside of the summer season, consistent with a seasonal shift in the relative costs and benefits of pigmentation. Second, using a continentally distributed predation experiment, we find that predation risk covaries with spatiotemporal variation in wing pigmentation and is linked to shifts in the local abundance of migratory birds. Overall, our analyses establish an eco-evolutionary link between tropical and temperate regions, underscoring the importance of considering both the evolutionary and ecological consequences of spatiotemporal variation in biotic interactions as species assemblages shift in response to global change.

Phenotypic differences among populations can arise through heritable genetic divergence, phenotypic plasticity, or both, making it difficult to determine whether trait-environment correlations observed in nature reflect adaptive evolution. Within threespine stickleback (Gasterosteus aculeatus) studies, numerous document morphological differences among allopatric-, parapatric-, and even sympatric populations. These phenotypic differences among populations are often correlated with diet and lake habitat (e.g., lake size), suggesting an adaptive value to the population differences. However, many studies of ecomorphological divergence in stickleback use wild-caught stickleback, which may differ due to evolution or plasticity. Although common garden experiments have confirmed that population differences can be heritable, such experiments typically entail small numbers of populations. Consequently, we still do not know to what extent well-known trait-environment correlations in stickleback are a result of evolution. To address this gap, we reared stickleback embryos from 27 lake populations on Vancouver Island, in a laboratory environment. Morphological differences among populations persist in common-garden fish, confirming a large role for divergent evolution. These heritable differences were associated with environmental variation among lakes, implying an adaptive value. However, some well-known trait-environment relationships in stickleback did not persist in common-garden fish and may be primarily plastic.

Parental qualities can influence the development and fitness of their offspring via genetic and non-genetic effects. Although these effects are often linked to parental phenotypes, the effect of parental genetic variation linked with relevant phenotypes is less well understood. We performed full factorial crosses based on parental genotypes for an age-at-maturity-related gene, vgll3, to investigate how the parental genotypes influence Atlantic salmon (Salmo salar) offspring survival, growth, and development in their early life. Beyond the connection with age at maturity, the additional association between vgll3 and body condition in Atlantic salmon offers a potential pathway by which the maternal vgll3 genotype could influence offspring early life fitness. Combined with measurements of maternal phenotype and egg characteristics, the crossing design therefore allowed us to disentangle the maternal and paternal genetic and non-genetic contributions to variation in offspring survival and phenotypic traits. The phenotypic traits measured were hatching length and yolk sac area, growth, and yolk sac consumption and conversion efficiency. Parental vgll3 genotype did not influence the majority of our measured egg traits or alevin traits except for a genetic effect of paternal vgll3 genotype on offspring survival, whereby the paternal late maturation allele was associated with higher survival. Maternal effects were strongest for survival and for traits associated with hatching and weaker for alevin growth and yolk sac usage. Paternal effects on the measured alevin traits were negligible. The results from our study demonstrate that both maternal and paternal effects have the potential to influence offspring early life fitness traits.

Dormancy is a widespread life-history strategy that enables organisms to persist through periods of adverse environmental conditions. Despite its prevalence, the evolutionary forces shaping dormancy and the timing of reactivation remain poorly understood, particularly in pathogens facing predictable environmental fluctuations. Here, we investigate how seasonal variation can drive the joint evolution of pathogen dormancy and reactivation, and whether these traits are favoured to evolve as fixed or plastic strategies. Using a theoretical model of vector-borne disease transmission, we show when seasonality can promote plasticity in dormancy and reactivation. The optimal timing of transitions between active and dormant states depends critically on the environmental cues available to pathogens and on their reliability for predicting future transmission opportunities. Although motivated by the biology of relapsing malaria parasites, our results provide a general framework for understanding the evolution of dormancy as an adaptive response to periodic environmental fluctuations across diverse pathogen systems.

Exaggerated sexually selected traits are known to be highly variable and their degree of expression is dependent on nutritional input. Yet the molecular mechanisms linking nutritional variation to phenotypic variation remain poorly understood. Here, we investigate how nutritional input shapes the development of male rear leg length, an exaggerated and highly variable trait in the water strider Microvelia longipes, using comparative transcriptomics and RNA interference gene knockdown experiments. We demonstrate that nutrition is the primary driver of gene expression variation, with male exaggerated rear legs exhibiting the highest number of nutrition-responsive genes. Moreover, the increase in morphological divergence between leg types or sex, which is systematically exacerbated by rich nutrition, is associated with increased number of leg-biased genes. These comparative analyses allowed us to identify BMP11 as specifically enriched in female and male rear legs. Knockdown of BMP11 abolishes nutritional plasticity in leg length only in males, positioning it as a key integrator of environmental, sex and developmental signals. Our findings reveal that transcriptional modulation provides a molecular interface between nutrition and trait exaggeration. This work advances our understanding of how environmental cues are translated into complex phenotypes and highlights the role of developmental plasticity as a substrate for evolutionary change.

Evolutionary theory predicts that fluctuating environments favor adaptations that maximize geometric-mean fitness by reducing variance in performance across conditions. We tested this prediction experimentally by evolving the lactic acid bacterium Lactococcus cremoris on the sugars fructose and galactose in density-controlled chemostats under four resource regimes: constant supply of fructose, constant supply of galactose, a constant mixture of both sugars, and a temporally alternating supply of the two. In the absence of temporal variation, trade-offs between fructose and galactose resulted in evolutionary divergence into a fructose specialist and a galactose specialist. In contrast, adaptation to temporal resource variation equalised growth performance on both sugars by increasing its growth rate on galactose and decreasing it on fructose. Interestingly, performance equalization emerged across replicate populations through distinct resource-transition strategies, indicated by differences in resource affinity and growth recovery on fructose and galactose among strains isolated from the evolved populations. Our results show that temporal resource variation selects for variance-minimizing resource adaptations while adopting multiple resource transition strategies, illustrating how distinct modes of metabolic plasticity can yield convergent fitness outcomes.

Assessing intraspecific variation in thermal stress tolerance is key to predicting plant responses and long-term persistence under climate change, yet its underlying sources and temporal dynamics remain poorly understood. Using a common garden experiment with four ecologically-relevant temperatures, we evaluated the sources and temporal dynamics of variation in temperature stress tolerance of 18 Lemna minor clonal lines from contrasting climates. Our results showed that past adaptation, physiological acclimation, and within-line variation jointly contributed to variation in performance. The study provides the first evidence of adaptive genetic differentiation in heat stress tolerance in this ecologically-widespread freshwater species, with lines from warmer regions showing higher growth under heat stress. However, these differences were transient and diminished under prolonged exposure. Experimental lines also showed acclimation over time, but these responses were strongly temperature-dependent and occurred only under sub-optimal conditions. Additionally, replicates from some lines exhibited divergent performance trajectories under sustained heat stress, suggesting the emergence of novel phenotypic variation, potentially mediated by epigenetic mechanisms. These results show that heat stress tolerance in L. minor arises from multiple interacting sources and is dynamically shaped by both selective history and immediate exposure time, suggesting a more nuanced, multi-layer understanding of variation in heat stress tolerance.

Understanding how populations persist in gradually deteriorating environments through evolution is a central question in ecology and evolutionary biology. Previous studies have primarily focused on identifying the critical rate of environmental change beyond which extinction is certain. However, the existence of a viable equilibrium when the rate is below the threshold does not guarantee that a population can survive the transient dynamics to reach it. Using a quantitative genetic model that explicitly incorporates feedback among population size, genetic variance, and mean trait evolution, we show that population persistence can exhibit bistability when the rate of environmental change is below the extinction threshold. Specifically, extinction still occurs if the initial population size and genetic variance fall below a critical level. The initial state also influences the eco-evolutionary dynamics, such that a temporary increase or decline in population size and/or genetic variance does not necessarily predict the ultimate fate of the population. Therefore, in addition to estimating the critical rate of environmental change for extinction, characterizing current population size, genetic variation, and the degree of maladaptation may improve predictions of extinction risk in deteriorating environments.

Chromosomal inversions are increasingly recognized as important drivers of local adaptation and ecological divergence because they suppress recombination and maintain adaptive allele combinations despite ongoing gene flow. However, the eco-evolutionary conditions favouring the establishment of such indirectly adaptive inversions, as well as the genomic features that distinguish them from other inversions remain incompletely understood. In this study, we investigated these questions in a wild sunflower system comprising two species: Helianthus debilis and Helianthus praecox, which exhibit diverse ecotypes and varying degrees of geographic overlap across Texas and Florida in the USA. To resolve the evolutionary relationships between and within these species, and identify potentially adaptive inversions, we generated haplotype-resolved reference assemblies and integrated comparative and population genomic analyses. We identified three major genetic clusters that only partially corresponded to taxonomic classifications. We further detected 156 inversions across the genome, 11 of which showed signatures consistent with a role in local adaptation. Notably, nine of the 11 putatively adaptive inversions were found in sympatric Texas populations. Together with a similar enrichment of inversions in genome assemblies from sympatric versus allopatric populations, our results suggest that inversions are more likely to evolve in heterogeneous environments with ongoing gene flow than in allopatry. Lastly, locally adaptive inversions were generally larger, contained more genes, and showed greater sequence divergence between haplotypes than other types of inversions. Our findings provide empirical support for the role of gene flow in promoting inversion establishment and identify genomic characteristics associated with indirectly adaptive inversions.

The relative importance of genetic drift versus selection to evolutionary change has long been debated. This debate has mainly focused over long-time-scales (e.g. hundreds of thousands of generations), leaving the question of short-term evolutionary change relatively unaddressed. Our knowledge about the effects of selection on genetic change over short time scales is often based on identifying major allele frequency changes at few loci with large selective advantage. Yet selection often acts on polygenic traits where the short-term response is shaped by small shifts in allele frequency at many loci that will be difficult to distinguish from genetic drift. Here, we quantify the genome-wide effects of polygenic selection over a single generation, using the idea that alleles in stronger genetic correlation (LD) with selected alleles are expected to show greater variance in allele frequency change than expected under genetic drift. We derive expressions relating variation in LD among loci to the variance in allele frequency change due to linked selection and genetic drift and leverage this theory to quantify the contribution of linked selection to a single generation of allele frequency change. To demonstrate our approach, we decompose the genome-wide allele frequency change in the UK Biobank using fitness proxy phenotypes. We show that selection makes a small, but significant, contribution, with genetic drift making up the large majority of the change in allele frequencies. Our framework could be applied to other organisms for which data on number of offspring or allele frequencies over consecutive generations are available, enabling investigations of the short-term, genome-wide effects of polygenic selection across a wide range of species.

Evolution of antibiotic resistance is a major global public health problem. Rapid emergence of antibiotic resistance is often linked to hypermutator bacteria with defective DNA repair, leading to high mutation rates that are broadly advantageous. However, depending on which DNA repair pathway is dysfunctional, mutators may sample only specific types of mutations at a higher rate. Thus, their mutation spectrum can be biased towards specific mutation types, influencing the identity of resistance mutations. Under strong antibiotic selection, an overall high mutation rate should generally shorten the time to sample a resistance mutation and increase the probability of resistance. However, recent work suggests that the mutation rate for specific types of mutations in target genes that drive high resistance is more important than the overall mutation rate. To systematically test this prediction, we exposed Escherichia coli mutators with varying mutation rates and spectra to antibiotics targeting different cellular functions. For each strain, we determined the highest antibiotic concentration at which resistance could emerge overnight, quantifying both the magnitude and probability of resistance. High level antibiotic resistance was generally better predicted by specific rather than overall mutation rate, and resistance mutations matched the mutation spectrum of the respective mutator. Despite the varying magnitude of resistance, at the highest antibiotic concentration survived by each strain, the respective resistance mutations were generally costly in the absence of antibiotic. Given that mutators often arise in laboratory, natural, and clinical settings under antibiotic selection, we suggest that their mutation spectra deserve more attention.

The distribution of fitness effects (DFE) of new mutations underpins our understanding of molecular evolution, mutation load and the maintenance of quantitative genetic variation. Most direct estimates in microbes rely on mutation-accumulation (MA) lines that harbour many mutations, so that only the mean and variance of the DFE can be inferred reliably and non-genetic ('environmental') differences between lines are usually ignored. Here we generated 192 Escherichia coli MA lines that accumulated no mutations, one mutation or more than one mutation in similar proportions. Comparing the growth rates of lines with mutations with the mutation-free controls allowed us to partition fitness variation into genetic and non-genetic components. We estimate the average selection coefficient of a single mutation is unlikely to be less than -0.0020 (with 95% credibility) - a value that is small, not significantly different from zero, and largely concordant with most previous estimates from multi-mutant MA studies, although those earlier results have often been misinterpreted as implying much larger deleterious effects. Crucially, systematic non-genetic effects among lines were an order of magnitude larger than mutational effects, and failure to model them would have biased the mean selection coefficient downwards by an order of magnitude. Our study demonstrates that spontaneous mutations in E. coli are typically only mildly deleterious and that rigorous controls for environmental effects are essential for unbiased inference of the DFE in microbial systems.

Tree populations can respond to climate change through migration, phenotypic plasticity, or genetic evolution. Despite long generation times of forest tree species, recent studies suggest that their evolutionary responses may occur rapidly. Using oaks as a model system, we synthesize evidence from 88 common garden studies and from historical, retrospective and longitudinal approaches to explore how populations have adapted to climatic variability across different biomes, and assess the consistency and pace of evolutionary responses across spatial and temporal climatic gradients. We found that approximately 61% of the studies exhibited significant differences among populations but climatic drivers and adaptive strategies differed among biomes. Temperature-related clines predominated in temperate regions, with populations from warmer origins showing longer growing seasons and higher growth potential. In seasonally dry biomes, aridity favored increased drought tolerance in Mediterranean populations but drought avoidance in tropical populations. Allochronic studies revealed genetic changes over decades to millenia in response to climate changes, with warming associated with increased growth and reduced specific leaf area in temperate oaks. Thus, spatial differentiation and temporal evolution were generally congruent in direction for most traits except for leaf unfolding, while short-term evolutionary rates exceeded long-term estimates by two to three orders of magnitude. In summary, provenance trials can provide useful information on the direction of climate-driven evolution for some traits, but may underestimate its contemporary pace. More studies are needed to evaluate whether standing genetic variation of forest tree species is sufficient to track current climate change.

Demographic processes such as colonization to new environments and gene flow fundamentally shape the genomic landscape, either facilitating or constraining the efficiency of selection by altering the balance between genetic diversity and adaptive responses. Although theoretical predictions suggest that the efficacy of selection is dictated by a species' demographic history, empirical studies often overlook these constraints, yielding misleading observations. In this study, we present the first functional genome annotation for the wood frog (Lithobates sylvaticus), providing a critical genomic resource for understanding the adaptive capacity of the species. Based on the annotation, we examined the potential for selection to drive genomic and phenotypic divergence among populations distributed across vernal ponds in Northeastern Connecticut, USA. A genotypexenvironment association analysis revealed that the frequency of an outlier loci (Rab28) spikes in response to one wetland that is notable for having relatively low canopy cover and large area. We also found that selection has driven a strong disparity in embryonic development among populations of wood frog at a rate exceeding that of neutral genetic drift. This genomic signature of selection together with a remarkable phenotypic differentiation suggests that natural selection overcomes the power of genetic drift, even in a landscape characterized by relatively recent colonization and substantial evidence of connectivity among breeding wetlands. These findings improve our understanding of the wood frog's variation at a microgeographic scale.