Evolution Letters

Demographic history can profoundly shape genomic variation by altering levels of inbreeding, the strength of genetic drift, and the efficacy of purifying selection, thereby influencing both the accumulation and expression of deleterious variation. Yet the extent to which these genomic consequences translate into organismal performance remains poorly understood. Here, we investigated how contrasting demographic histories shape genomic diversity, inbreeding, genetic load, and performance across mainland and insular populations of the Italian wall lizard, Podarcis siculus. Using whole-genome sequence data from 263 wild-caught individuals and field-based performance measurements from 134 lizards, we characterised population structure and demographic history, quantified genomic diversity, runs of homozygosity, and deleterious variation, and tested associations between genomic inbreeding and performance traits. Island populations showed reduced genetic diversity, increased autozygosity, and elevated genetic load relative to mainland populations, consistent with stronger genetic drift and reduced efficacy of purifying selection. Patterns of deleterious variation were consistent with purging of strongly, but not mildly, deleterious variants. Greater genomic autozygosity was associated with reduced bite force in island lizards, a pattern consistent with inbreeding depression, whereas sprint speed, sperm quality, immunocompetence, and spatial cognition showed no significant association with inbreeding. Genome-wide mapping of runs of homozygosity further identified multiple genomic regions associated with reduced bite performance. Together, these results show how demographic history shapes genomic diversity, homozygosity, and deleterious variation in wild vertebrate populations, while revealing that phenotypic consequences can be trait-specific, a pattern that may reflect differences in genetic architecture and the extent of environmental influence on trait variation.

Global warming will impact natural selection on plant traits and their plasticity by influencing phenotypes, biotic interactions, and fitness. Because warming affects biotic interactions, community composition may influence how warming affects selection on plants, but this is little studied. We grew full-sibling pairs of Brassica rapa plants in an ambient and hot temperature environment and exposed them to visitation by a pollinator (Bombus terrestris), a pollinating herbivore (Pieris rapae), or their combination. We recorded plant phenotypes, insect visitation, herbivory, and plant fitness. We used these to calculated phenotypic selection on plant traits and their plasticity, including additive and nonadditive effects. Elevated temperature changed selection on traits related to pollinator attraction, such as flower number, nectar production, and floral scent emission. We found both positive and negative selection on temperature-mediated trait plasticity depending on the biotic treatment. Elevated temperature changed patterns of additive and non-additive selection on a variety of traits including flower morphology and scent. This study shows that elevated temperatures can reshape patterns of phenotypic selection, including nonadditive effects, and plastic trait expression. Effects of elevated temperature on phenotypic selection depended on the biotic interactors, highlighting the importance of community context for the effects of warming on natural selection.

How natural populations maintain genetic variation for fitness remains a central problem in evolutionary biology. Theory predicts that opposing selective pressures across environments can preserve fitness-associated polymorphism, but how interactions among species contribute to this process remains poorly understood. Here we show that host diversity preserves standing genetic variation within sexual populations of the leafmining fly Scaptomyza flava. We evolved twelve populations for ten generations on either of two naturally co-occurring host plants or on both, pooling survivors from the two hosts before mating. Single-host populations evolved reciprocal fitness trade-offs, whereas two-host populations maintained relatively even performance across hosts. Whole-genome time series dynamics identified a linked region in which alleles increased on one host and decreased on the other, while showing little net change under two-host conditions. Wild flies reared from the two hosts showed corresponding allele-frequency differences within this region. Across the genome, two-host populations retained more rare variants than populations evolving on either host alone. These findings show that selection imposed by different host species in sympatry can maintain standing genetic diversity within an herbivore population.

Species interactions shape ecological dynamics, but adaptation to one interaction can trade off with others. Experiments that measure such evolved fitness changes across multiple interactions remain rare. We used experimental evolution to test whether recent selection under one ecological interaction changes fitness under other interactions in a fly-parasitoid system. We evolved a genetically diverse Drosophila melanogaster population for 15-17 generations under three regimes: benign conditions (control), high intraspecific competition, and infection by the parasitoid wasp Leptopilina boulardi. We then measured fly fitness (egg-to-adult survival and subsequent reproduction) under benign conditions, high intraspecific competition, and infection by three other parasitoid species and an additional conspecific L. boulardi strain. Selection history strongly influenced fitness across interactions. Populations maintained under high larval density showed reduced survival under infection by L. boulardi and L. victoriae, indicating a trade-off between past selection for competition and defence against some parasitoids. Populations evolved under parasitoid infection by L. boulardi showed increased resistance to a conspecific strain but reduced fitness when infected by another species, L. heterotoma. Our results show that rapid evolution in response to a single interaction can reshape multiple ecological interactions through fitness trade-offs, highlighting how recent evolutionary history may influence community dynamics and invasion susceptibility.

Extreme climatic events (ECEs) could potentially induce episodes of rapid adaptive evolution, altering the evolutionary trajectories and viability of wild populations experiencing increasingly stochastic environments. Adaptive potential stems substantially from additive genetic variance (V) in survival. However, the degree to which ECEs impact this variance, and the resulting evolutionary implications, have not been fully conceptualised or quantified in nature. These aims are highly challenging because underlying genetic and environmental variances have fundamentally non-linear effects on the dichotomous phenotypic outcome of survival versus death, while substantial data are required for estimation. We present a conceptual and analytical framework that formalises biological hypotheses for how V depends on environmental severity, how such dependences are reshaped by non-linear genotype-environment-phenotype relationships and demographic structure, and the implications for evolutionary responses. We then use 25 years of survival and pedigree data from European shags (Gulosus aristotelis) to decompose variance in adult survival across diverse environmental conditions including ECEs. Using a capture-recapture animal model, we demonstrate non-negligible V underlying adult survival across all years combined, implying notable adaptive potential. Yet, partitioning by environmental severity revealed substantial V in good years with high survival but negligible V in bad years with ECE-induced low survival, implying a genotype-by-environment interaction that constrains adaptive potential under severe conditions. However, scale transformations showed how the non-linear genotype-environment-phenotype relationship can distort or even reverse such patterns, by reducing the extent to which V is phenotypically expressed in good conditions with high mean survival and amplifying it in more severe conditions with lower mean survival. Evolutionary responses to severe conditions could consequently be non-negligible even given small underlying V. We thereby demonstrate how ECEs can reshape adaptive potential, highlighting the need to integrate impacts of environmental severity on genetic variation in fitness components into predictions of population resilience under climate change.

Host-microbiota interactions are crucial in adapting to environmental changes, such as fluctuating energy availability. Yet, the extent to which hosts and their microbiota exhibit coordinated plasticity in response to transient energy limitation remains unclear. Here, we examined the capacity for parallel reversible plasticity in hosts and gut microbiota to temporary dietary restriction in hosts with differing energy needs. We subjected bank voles (Clethrionomys glareolus) from a long-term artificial selection experiment for high aerobic metabolism (A-lines) and control lines (C-lines) to dietary restriction (food dilution with insoluble fiber) followed by a recovery period. We measured traits relevant for vole energy consumption and fecal microbiota composition at baseline, after dietary restriction, and after recovery. We hypothesized that A-line voles would experience more severe and prolonged physiological effects of dietary restriction than C-line voles, which might be counteracted by higher microbiota responsiveness. Dietary restriction caused a temporary increase in food consumption, decrease in body mass and resting metabolic rate, and significant shifts in gut microbiota composition, all of which returned to near baseline levels during the recovery period. These effects were largely similar for the selection lines, but contrary to our prediction, the effect of dietary restriction on bacterial diversity was stronger in C-lines. This suggests higher resistance of the A-line microbiota to dietary changes, perhaps resulting from increased host control over microbial communities due to the directional selection for high metabolic capacity. Overall, our findings highlight a substantial capacity for reversible plasticity in host physiology and gut microbiota in fluctuating environments.

Mutation-selection balance is the most plausible general mechanism for the maintenance of additive genetic variance (VA) for quantitative traits in natural populations. It is well established that the genetic variants affecting traits (QTLs) are widely distributed across species' genomes. At the same time, unconditionally deleterious mutations are also expected to be common, with those with the largest fitness effects tending to be strongly recessive. Many genomes possess regions of restricted recombination that could result in tight linkage between largely recessive deleterious alleles, conditions which can lead to elevated heterozygosity via associative overdominance (AOD). Here we show that weakly selected QTLs linked to genomic regions exhibiting AOD can elevate VA above what is expected in the absence of unconditionally deleterious mutations. Selection on traits when VA is maintained by AOD, however, may expose recessive deleterious alleles as homozygotes, reducing fitness. Thus, while AOD may contribute to the maintenance of VA, variation maintained in this way may not be readily accessible by natural or artificial selection.

The repeated evolution of similar phenotypes in response to shared ecological pressures provides striking examples of natural selection and raises broader questions about the predictability of evolution. Evolutionary constraint may shape this predictability, while the apparent extent of parallelism may also depend on the biological scale at which it is measured. When are adaptive solutions channeled along the same route? We addressed this question using three sympatric benthic-limnetic ecotype pairs of threespine stickleback (Gasterosteus aculeatus), characterizing gene expression in gill and liver from wild-caught fish. We tested whether proxies of pleiotropic and coding-sequence constraint predicted the repeatability of transcriptional divergence across lakes. At the gene level, differential expression was strongly biased toward parallel rather than antiparallel responses. At the functional level, numerous pathways showed parallel enrichment, but the conservation of their underlying member-gene responses varied substantially, indicating that similar functional outcomes can arise with differing degrees of gene-level concordance. Most importantly, several proxies of evolutionary constraint predicted transcriptional repeatability, particularly in gill: broadly expressed, highly connected, and more slowly evolving genes showed more stable expression responses across lakes, with similar relationships evident for repeated use of genes within functionally parallel pathways. Together, these results show that both gene-level constraint and biological scale contribute to variation in molecular repeatability and suggest that the predictability of repeated adaptation may reflect an interaction between genetic architecture, population-genetic context, and the level of biological organization at which parallelism emerges.

Genotype-environment association (GEA) approaches identify genetic variants that likely contribute to adaptation along environmental gradients. These associations can inform predictive models of maladaptation risk and evolutionary rescue in future climates. However, because population structure and climate parameters often co-vary, tradeoffs arise between accounting for population structure to reduce false positive associations and removing true positives. Here, we examine whether conducting GEA analyses at multiple spatial scales provides more informative associations by mitigating confounds between population structure and environment, and we evaluate what factors influence how congruent GEA results are across regions. We performed GEA analyses for climate parameters on genome resequencing data obtained for 110 annual populations of the common monkeyflower, Mimulus guttatus. We find that more genetic variation was specifically attributable to environmental variation in regional GEA models compared to a full-range model, and that agents of selection differ considerably in importance among regions and range-wide. Few genetic targets of selection shared across regions were detected, yet all regions possess ample standing genetic variation for most environment-associated variants, suggesting that regional differences in climate breadth may be a primary cause of this incongruence. In combination with a genome-wide association study for several climate-associated phenotypes, we also find that regulators of flowering repressors in the FLC/MAF gene family often harbor adaptive variation in this species. Together, our results suggest that GEA analyses of widespread species considerably benefit from examining both range-wide and regional trends to more fully capture and understand the agents and targets of climate adaptation.

Populations that have detectable additive genetic variance for fitness (VA(W)) have the capacity for increase in their mean fitness through natural selection. The extent to which the magnitude of VA(W) in wild populations is predictive of the rate of adaptation is not well known, because few empirical field-based studies have been designed to address this question. Here, we report a two-year field experiment with pedigreed seeds embedded in four natural populations of the annual wildflower Baby Blue Eyes (Nemophila menziesii H. & A.), a species native to western North America. We first estimated VA(W) in a parental generation and then evaluated whether that estimate accurately predicted the adaptive response observed in the subsequent offspring generation grown under natural field conditions. We achieved this by directly comparing the mean fitnesses of the parental generation and their progeny grown under the same environmental conditions. We detected VA(W) and evidence of adaptation in all populations despite inter-annual differences in environmental conditions that directly affected fitness. Genotype-by-year interactions in fitness indicate that the fitness ranking of families differed between years, implying that the selective environment shifted over time. Additionally, although the environment in the second year reduced population mean fitness in three sites, the offspring generation maintained mean fitness at or above replacement, suggesting that adaptive evolution may have buffered the effects of environmental change. Overall, our results suggest that the four populations harbored sufficient VA(W) for adaptation through natural selection to the environmental conditions observed during the two years of this study.

Random genetic drift, rather than selection, is expected to determine the dynamics of alleles with fitness effects that fall below the reciprocal of effective population size (Ne). This is the drift barrier. The drift barrier hypothesis suggests that adaptation may be hopelessly constrained in organisms with low Ne, with much of the complexity of life reflecting a byproduct of ineffective natural selection. Yet decades of empirical research in evolutionary ecology provides substantial evidence of adaptation in finite metazoan populations. Here I explore the extent to which the drift barrier may, or may not, constrain contemporary adaptive divergence under directional selection in the wild. Compensatory directional selection on polygenic traits occurring after the fixation of a deleterious allele will be twice as efficient compared to the initial action of stabilizing selection. Consistent with this result, meta analysis reveals a negative relationship between contemporary estimates of Ne and the strength of directional selection in natural populations. Analysis of empirical phenotypic selection gradients from wild metazoans further reveals that directional selection is often strong enough to overcome the constraints imposed by finite population size, across a range of genetic architectures. Moreover, on a multi-peak adaptive landscape, the probability of a peak shift between adaptive zones increases exponentially as Ne declines, with observed values of contemporary Ne typically being well within the range needed for peak shift models to be a viable explanation of diversity. Together, these results suggest that widespread adaptation in metazoans is not inconsistent with the fundamental constraints on perfection imposed by drift.

Chromosomal inversions are proposed to aid local adaptation to divergent habitats when there is gene flow by creating regions of low recombination that can maintain tight linkage between multiple locally adaptive alleles. However, key theoretical predictions about the role of chromosomal inversions in local adaptation remain largely untested in empirical systems. Here, we test the prediction that inversions will concentrate relatively small genetic effects across multiple ecologically relevant traits by exploring inversion-phenotype associations of three inversions in threespine stickleback (Gasterosteus aculeatus). Using complementary approaches of association mapping in wild-caught individuals and genetic mapping in lab-raised individuals from two divergent genomic backgrounds, we found that an inversion on chromosome XXI influences multiple ecologically relevant traits. The inversion has small-to-moderate effects on these traits, as expected for inversions involved in polygenic adaptation. Further consistent with theoretical predictions, inversion heterozygotes show intermediate phenotypes. While most inversion-phenotype associations are consistent across different genomic backgrounds and experimental approaches, some inversion-phenotype associations were specific to a single dataset. These results indicate that the phenotypic effects of inversions are shaped by both genomic and environmental context, which could facilitate population-specific adaptation. Together, these results support the role of the chromosome XXI inversion in ecological divergence in threespine stickleback. More broadly, our results suggest that inversions can contribute to local adaptation by preserving linkage between small-effect adaptive alleles despite extensive gene flow.

Plasticity has been proposed to facilitate the evolution of novelty, but it's unclear if it can drive a transition to a novel kind of individual. We report the experimental evolution of obligate somatic differentiation in Eudorina, a predominantly undifferentiated species that develops plastic somatic cells in response to cold stress. Eudorina is a species of volvocine algae, a clade in which cellular differentiation has evolved repeatedly. We exposed Eudorina from 2 lab lines and 46 course-based undergraduate research experience lines to repeated cold shock. Somatic differentiation evolved rapidly, with 21 of 48 lines (44%) exhibiting a larger proportion of differentiated colonies in baseline conditions. We also identified a lineage with obligate somatic differentiation; this is the first published example of the experimental evolution of obligate somatic differentiation. 11 lines, including the obligately differentiated one, also exhibited changes in the proportion of somatic cells per differentiated colony. The proportion of somatic cells in these lines converged with that of Pleodorina, a polyphyletic soma-differentiated volvocine algae genus. Genome sequencing revealed that 93% of genes mutated in the obligately differentiated line and not in the control had at least one homolog with soma-specific expression in obligately differentiated Volvox carteri or Astrephomene gubernaculifera and/or cold-induced expression in unicellular Chlamydomonas reinhardtii. Moreover, 72% of genes mutated in the obligately differentiated line and not in the control had homologs with both soma-specific expression and cold-induced expression. These genes all have regulatory mutations and lie at the intersection of cold shock and somatic differentiation regulatory modules. Our results provide the first empirical demonstration that the modification of plastic responses to the environment can drive the evolution of somatic differentiation, a key step in the evolution of a new kind of evolutionary individual.

Heritable variation in microbiome composition could theoretically evolve in response to selection acting on hosts, but empirical evidence of this is scarce. We tested for effects of allelic variation in Boechera stricta on microbiome composition and downstream consequences for host fitness. In the greenhouse, near-isogenic lines with contrasting phytochemistry alleles differentially conditioned soil microbiota in ways that changed the relative fecundity of host genotypes. In the field, root microbiome differences mediated allelic effects on host fitness. Selection gradients on individual taxa and multivariate axes of root microbiome composition suggest that independent components of the bacterial community favor each allele, especially under drought. These results show that microbiota contribute to natural selection on a major-effect phytochemistry gene, empirically closing the loop between microbiome heritability and host trait evolution.

Dominance is an important and evolvable property of the genotype-phenotype map. A longstanding debate in evolutionary genetics concerns whether dominance is determined primarily by intrinsic properties of alleles at the focal locus or by modifiers elsewhere in the genome. Theoretical models show that second-site modifiers of dominance can evolve under some conditions. However, direct empirical tests of these models are rare because they require holding the focal heterozygous genotype constant while changing the rest of the genome. In the Drosophila montium species subgroup, female pigmentation is a Mendelian trait controlled by a single gene, POU domain motif 3 (pdm3), but the dominance relationships between pdm3 alleles differ among species. Using reciprocal introgressions among three closely related species, we compared females carrying the same Light/Dark pdm3 allele combinations in different homozygous or heterozygous genomic backgrounds and across different temperatures. In both species-pair comparisons, changing genomic background significantly altered the phenotype of identical pdm3 heterozygotes, demonstrating the existence of second-site modifiers of dominance. The effects of dominance modifiers depend on the particular pair of pdm3 alleles and on rearing temperature. These results show that dominance in this system is a genotype-by-genotype-by-environment trait, rather than a fixed attribute of individual alleles. The finding that second-site modifiers can alter dominance by reshaping reaction norms provides a developmental mechanism that links the evolution of dominance to phenotypic plasticity.

Assortative mating for a trait under selection can increase the rate of adaptive evolution and limit introgression of detrimental alleles. We therefore hypothesized that assortative mating facilitated the rapid evolution of flowering phenology observed in the self-incompatible perennial Lythrum salicaria (purple loosestrife) as it invaded eastern North America. We characterized flowering schedules of 600 individuals representing 20 populations sampled along a latitudinal gradient of 10 degrees and grown in a common garden at mid-latitude. Consistent with our hypothesis, we found that flowering schedules were less synchronous in the mixed population of the common garden (s = 0.50) relative to the 20 locally adapted populations comprising it (s = 0.56 to 0.86), and flowering synchrony decreased towards higher latitudes of origin. Despite high synchrony, assortment potential ({rho}) by growth and phenology varied by population ({rho} = 0.03 to 0.61), but the predicted negative correlation between s and {rho} was masked by among-individual fitness variation in the common garden. We show how fitness variation and asynchrony associated with locally adapted phenology can reduce the fitness impacts of maladaptive gene flow and accelerate the rate of adaptive evolution during invasion.

Domestication is an evolutionary process that can begin before deliberate breeding, when association with humans reshapes gene flow and selection. The yellow mealworm, Tenebrio molitor, is undergoing this transition from a synanthropic pest of stored grain to farmed species. We asked whether gene flow between farmed populations contributes to adaptation to captivity and whether selection extends to production traits. We combined population genomics of 320 beetles from eight farmed and wild populations with genetic mapping of 15 production traits from 3,575 individuals. Farm stocks retained high diversity and weak differentiation, with Netherlands-related ancestry connecting populations across Europe and Canada. Farm-restricted sweep-like signatures were 2.06-fold enriched within regions of excess allele sharing, suggesting local selection on introgressed variation. Across 305 production-trait QTLs, overlaps with selection and introgression signals showed no significant enrichment or depletion, suggesting that adaptive gene flow may primarily contribute to adaptation to captivity rather than broadly shaping growth, development and fertility. Nevertheless, egg-hatching-rate and development-time QTLs overlapped regions of reduced nucleotide diversity and low Tajima's D. These findings support a model in which gene flow supplies variation for unintended selection under intensive rearing. Crowding and physiological stress may favour adaptation to captive environments before sustained breeding establishes a broad genomic response at production loci.

Variation in abiotic and biotic factors drives unique coevolutionary trajectories, yet we know little about how individual and interactive effects from such environmental factors alter the genomic basis of coadaptation. As a follow-up study after 6 generations of experimental coevolution, we analyzed whole-genome re-sequencing data from fast-cycling Brassica rapa plants that coevolved with a pollinating herbivore (Pieris rapae butterflies) in two different temperature environments (ambient/elevated) and in the presence/absence of bumblebees that did not coevolve. We found that genomic divergence between plant populations coevolving in the presence or absence of bumblebees was larger relative to plant populations coevolving in different temperature environments. Next, we found that the presence of bumblebees affected the number of genomic regions under selection differently depending on which temperature environment plants coevolved in. More specifically, we found no genomic regions under selection when plants coevolved in elevated temperatures and in the absence of bumblebees, but the most genomic regions under selection when plants coevolved in elevated temperatures and in the presence of bumblebees. Finally, genomic evolution underlying defense traits was larger when plants coevolved in the presence of bumblebees relative to when plants coevolved in the absence of bumblebees, which fits the prediction of coevolution being more antagonistic in the presence of a non-herbivorous co-pollinator. Overall, our results highlight how modifications in temperature and community context, potentially stemming from global environmental change, will affect the genomic basis of coevolution.

Populations adapting to heterogeneous environments often harbor many alleles that covary with environmental gradients, yet how so many adaptive variants can be maintained and show signatures of local adaptation remains unclear. Epistatic non-additive interactions among alleles may concentrate fitness effects at specific allelic combinations to shape complex traits and facilitate adaptation. We evaluate compositional epistasis among three intronic SNPs in the couch potato (cpo) gene, each independently clinal along the North American latitudinal gradient, using recombinant outbred populations fixed for distinct three-locus combinations. Flies carrying all three temperate alleles (cpoTTA) or all three tropical alleles (cpoCGT) show non-additive increases in traits associated with fitness in their respective environments: dormancy, starvation resistance, and lipid storage in temperate flies and fecundity in tropical flies. Intermediate genotype combinations generally show weaker and negative deviations from additive predictions. Temperate genotypes show reduced cpo expression and independently create predicted transcription factor binding sites, suggesting a regulatory basis for the observed phenotypic effects. Consistent with selection shaping haplotype frequencies against a backdrop of ongoing recombination, the temperate and tropical genotypes are enriched above random expectation across the latitudinal cline, with directionally consistent but non-significant seasonal patterns. Our findings demonstrate that non-additive interactions among non-coding variants within a single gene can produce large, pleiotropic fitness effects and shape genotype distributions in natural populations, providing a mechanism by which a small number of regulatory variants can underlie complex climatic adaptation.

Whether sexual selection facilitates or hinders adaptation to novel environments is a question of fundamental importance due to current rapid environmental change. Using phylogenetic comparative analysis in 42 Drosophila species, we found that sperm length - a sexually selected ornament - positively associates with the ability of males to survive high temperatures. However, the ability to remain fertile does not increase with sperm length to the same extent, meaning that longer sperm species experience a larger gap between temperatures that kill and temperatures that sterilize males. The findings are consistent with the idea that strong sexual selection on condition-dependent exaggerated traits may facilitate somatic resilience to environmental stressors, but that susceptibility to heat-induced infertility may be a cost of extreme sperm ornamentation. Overall, the data suggests multifaceted links between postcopulatory sexual selection and climate change.