Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late‐season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.     

Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs

Host organisms are believed to evolve defense mechanisms (i.e., resistance and/or tolerance) under selective pressures exerted by natural enemies. A prerequisite for the evolution of resistance and tolerance is the existence of genetic variation in these traits for natural selection to act. However, selection for resistance and/or tolerance may be constrained by negative genetic correlations with other traits that affect host fitness. We studied genetic variation in resistance and tolerance against parasitic infection and the potential fitness costs associated with these traits using a novel study system, namely the interaction between a flowering plant and a parasitic plant. In this system, parasitic infection has significant negative effects on host growth and reproduction and may thus act as a selective agent. We conducted a greenhouse experiment in which we grew host plants, Urtica dioica, that originated from a single natural population and represented 20 maternal families either uninfected or infected with the holoparasitic dodder, Cuscuta europaea. that originated from the same site. We calculated correlations among resistance, tolerance, and host performance to test for costs of resistance and tolerance. We measured resistance as parasite performance (quantitative resistance) and tolerance as the slopes of regressions relating the vegetative and reproductive biomass of host plants to damage level (measured as parasite biomass). We observed significant differences among host families in parasite resistance and in parasite tolerance in terms of reproductive biomass, a result that suggests genetic variation in these traits. Furthermore, we found differences in resistance and tolerance between female and male host plants. In addition, the correlations indicate costs of resistance in terms of host growth and reproduction and costs of tolerance in terms of host reproduction. Our results thus indicate that host tolerance and resistance can evolve as a response to infection by a parasitic plant and that costs of resistance and tolerance may be one factor maintaining genetic variation in these traits.     

Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive

Evolutionary biologists explain the maintenance of intermediate levels of defense in plant populations as being due to trade-offs, or negative genetic covariances among ecologically important traits. Attempts at detecting trade-offs as constraints on the evolution of defense have not always been successful, leading some to conclude that such trade-offs rarely explain current levels of defense in the population. Using the agricultural pest Ipomoea purpurea, we measured correlations between traits involved in defense to glyphosate, the active ingredient in Roundup, a widely used herbicide. We found significant allocation costs of tolerance, as well as trade-offs between resistance and two measures of tolerance to glyphosate. Selection on resistance and tolerance exhibited differing patterns: tolerance to leaf damage was under negative directional selection, whereas resistance was under positive directional selection. The joint pattern of selection on resistance and tolerance to leaf damage indicated the presence of alternate peaks in the fitness landscape such that a combination of either high tolerance and low resistance, or high resistance and low tolerance was favored. The widespread use of this herbicide suggests that it is likely an important selective agent on weed populations. Understanding the evolutionary dynamics of herbicide defense traits is thus of increasing importance in the context of human-mediated evolution.     

Antagonistic pleiotropy and mutation accumulation contribute to age‐related decline in stress response

As organisms age, the effectiveness of natural selection weakens, leading to age‐related decline in fitness‐related traits. The evolution of age‐related changes associated with senescence is likely influenced by mutation accumulation (MA) and antagonistic pleiotropy (AP). MA predicts that age‐related decline in fitness components is driven by age‐specific sets of alleles, nonnegative genetic correlations within trait across age, and an increase in the coefficient of genetic variance. AP predicts that age‐related decline in a trait is driven by alleles with positive effects on fitness in young individuals and negative effects in old individuals, and is expected to lead to negative genetic correlations within traits across age. We build on these predictions using an association mapping approach to investigate the change in additive effects of SNPs across age and among traits for multiple stress‐response fitness‐related traits, including cold stress with and without acclimation and starvation resistance. We found support for both MA and AP theories of aging in the age‐related decline in stress tolerance. Our study demonstrates that the evolution of age‐related decline in stress tolerance is driven by a combination of alleles that have age‐specific additive effects, consistent with MA, as well as nonindependent and antagonistic genetic architectures characteristic of AP.     

Selection and genetic (co)variance in bighorn sheep

Genetic theory predicts that directional selection should deplete additive genetic variance for traits closely related to fitness, and may favor the maintenance of alleles with antagonistically pleiotropic effects on fitness-related traits. Trait heritability is therefore expected to decline with the degree of association with fitness, and some genetic correlations between selected traits are expected to be negative. Here we demonstrate a negative relationship between trait heritability and association with lifetime reproductive success in a wild population of bighorn sheep (Ovis canadensis) at Ram Mountain, Alberta, Canada. Lower heritability for fitness-related traits, however, was not wholly a consequence of declining genetic variance, because those traits showed high levels of residual variance. Genetic correlations estimated between pairs of traits with significant heritability were positive. Principal component analyses suggest that positive relationships between morphometric traits constitute the main axis of genetic variation. Trade-offs in the form of negative genetic or phenotypic correlations among the traits we have measured do not appear to constrain the potential for evolution in this population.     

Genetic variation and covariation for resistance and tolerance to Cucumber mosaic virus in Mimulus guttatus (Phrymaceae): a test for costs and constraints

Genetic variation for resistance and tolerance to pathogens may be maintained by costs represented as genetic tradeoffs between these traits and fitness. The evolution of resistance and tolerance also may be constrained by negative genetic correlations between these defense systems. Using a complete diallel, we measured genetic variation and covariation for and among performance, resistance, and tolerance traits in Mimulus guttatus challenged with a generalist pathogen, Cucumber mosaic virus (CMV). Viral coat protein was detected by enzyme-linked immunosorbent assay (ELISA) in all inoculated plants, indicating that all plants were susceptible to infection, although the ELISA absorbance varied quantitatively across plants. Plants inoculated with CMV had significantly reduced aboveground biomass and flower production relative to controls, although date of first flower was unaffected by infection. All three of these performance traits showed moderate to high narrow-sense heritability (h2 = 0.32-0.62) in both inoculated and control plants. We found phenotypic variation for both tolerance of and resistance to our strain of CMV, but both displayed very low narrow-sense heritability (h2 < 0.03). We found no evidence of a trade-off between resistance and tolerance. We also found no evidence for a cost of resistance or tolerance. In fact, a significant genetic correlation suggested that plants that were large when healthy had the greatest tolerance when infected. Significant, positive genetic correlations found between performance of uninfected and infected plants suggested that selection would likely favor the same M. guttatus genotypes whether CMV is present or not.     

A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies

Resistance and tolerance represent two general strategies of plant defence against herbivores. Since resources available for allocation to defence are limited and resistance and tolerance are likely to serve the same functions for plants, the occurrence of trade offs between these two strategies has been assumed. We review the empirical evidence for tolerance–resistance tradeoffs by means of meta‐analysis of genetic correlations between resistance and tolerance obtained from 31 ecological and agricultural studies published during 1980–2003 and conducted on 17 different plant species. The sign of the relationship between tolerance and resistance differed depending on the type of plants examined. Tolerance and resistance tended to be positively correlated in crops and negatively correlated in wild plants, but the mean correlation coefficients in both plant types were not significantly different from zero. The magnitude of correlations was affected neither by the tolerance measure (reduction in growth or in fitness in damaged plants) nor by the resistance measure used (inverse of damage, antibiosis, antixenosis, or specific resistance trait). In wild plants correlations between resistance and tolerance were significantly negative (r=?0.069) only in studies where resistance was assessed as a specific chemical or mechanical resistance trait, but this correlation is based only on two studies. No difference in the mean resistance–tolerance correlations was found between studies conducted in the field and in the greenhouse; in both cases mean correlations tended to be positive. The results of our analysis indicate that conditions under which a negative association between resistance and tolerance occurs and, thus, the evolution of multiple defensive strategies in plants is constrained, are much more restrictive than previously assumed. However, the currently available studies are still scarce and taxonomically skewed to allow a thorough analysis of sources of variation in resistance–tolerance relationship. Specifically, we need more studies examining the relationship between specific resistance and tolerance traits, studies on perennial plants and under different environmental conditions.     

Genetic variation in variability: Phenotypic variability of fledging weight and its evolution in a songbird population

Variation in traits is essential for natural selection to operate and genetic and environmental effects can contribute to this phenotypic variation. From domesticated populations, we know that families can differ in their level of within‐family variance, which leads to the intriguing situation that within‐family variance can be heritable. For offspring traits, such as birth weight, this implies that within‐family variance in traits can vary among families and can thus be shaped by natural selection. Empirical evidence for this in wild populations is however lacking. We investigated whether within‐family variance in fledging weight is heritable in a wild great tit (Parus major) population and whether these differences are associated with fitness. We found significant evidence for genetic variance in within‐family variance. The genetic coefficient of variation (GCV) was 0.18 and 0.25, when considering fledging weight a parental or offspring trait, respectively. We found a significant quadratic relationship between within‐family variance and fitness: families with low or high within‐family variance had lower fitness than families with intermediate within‐family variance. Our results show that within‐family variance can respond to selection and provides evidence for stabilizing selection on within‐family variance.     

Plant chemical defence allocation constrains evolution of local range

Many species of plants in the wild are distributed spatially in patches, the boundaries of which may occur and change because of a complicated interplay between myriad environmental stressors and limitations of, or constraints on, plant coping mechanisms. By examining genetic variation and co‐variation among marker‐inferred inbred lines and sib‐families of an upland wild mustard species within and just a few meters across a natural patch boundary, we show that the evolution of tolerance to the stressful environment outside the patch may be constrained by allocation to glucosinolate compounds (GS) that are defensive against generalist insect herbivores. Several potential stressors were associated with the patch boundary, but carbon isotope ratios indicated that sib‐families with smaller stomatal apertures maintained performance better in response to late season dry conditions, suggesting that drought was an important stressor. The presence of GS may help explain the characteristic patchy distribution of mustards, a relatively diverse and important plant family. This result challenges one end of the continuum of the long‐standing Plant Apparency hypothesis, which essentially states the opposite causation, that low molecular weight toxins like GS are evolutionary responses of patchy distributions and correlated life‐history traits.     

THE COSTS AND BENEFITS OF TOLERANCE TO COMPETITION IN IPOMOEA PURPUREA,THE COMMON MORNING GLORY

Tolerance to competition has been hypothesized to reduce the negative impact of plant–plant competition on fitness. Although competitive interactions are a strong selective force, an analysis of net selection on tolerance to competition is absent in the literature. Using 55 full/half‐sibling families from 18 maternal lines in the crop weed Ipomoea purpurea, we measured fitness and putative tolerance traits when grown with and without competition in an agricultural field. We tested for the presence of genetic variation for tolerance to competition and determined if there were costs and benefits of this trait. We also assessed correlations between tolerance and potential tolerance traits. We uncovered a fitness benefit of tolerance in the presence of competition and a cost in its absence. We failed to detect evidence of additive genetic variation underlying tolerance, but did uncover the presence of a significant maternal‐line effect for tolerance, which suggests its evolutionary trajectory is not easily predicted. The cost of tolerance is likely due to later initiation of flowering of tolerant individuals in the absence of competition, whereas relative growth rate was found to positively covary with tolerance in the presence of competition, and can thus be considered a tolerance trait.     

The evolution of tolerance to damage in Gentianella campestris: natural selection and the quantitative genetics of tolerance

In the framework of phenotypic plasticity, tolerance to browsing can be operationally defined as a norm of reaction comparing plant performance in undamaged and damaged conditions. Genetic variation in tolerance is then indicated by heterogeneity in the slopes of norms of reaction from a population. We investigated field gentian (Gentianella campestris) tolerance to damage in the framework of phenotypic plasticity using a sample of maternal lines from natural populations grown under common garden conditions and randomly split into either a control or an artificial clipping treatment. We found a diversity of tolerance norms of reaction at both the population and family level: the impacts of clipping ranged from poor tolerance (negative slope) to overcompensation (positive slope). We detected heterogeneity in tolerance norms of reaction in four populations. Similarly, we found a variety of plastic architectural responses to clipping and genetic variation in these responses in several populations. Overall, we found that the most tolerant populations were late flowering and also exhibit the greatest plastic increases in node (meristem) production in response to damage. We studied damage-imposed natural selection on plasticity in plant architecture in 10 of the sampled populations. In general, there was strong positive direct selection on final number of nodes for both control and clipped plants. However, the total selection on nodes (direct + indirect selection) within each treatment category depended heavily on the frequency of damage and cross-treatment genetic correlations in node production. In some cases, strong correlated responses to selection across the damage treatment led to total selection against nodes in the more rare environment. This could ultimately lead to the evolution of maladaptive phenotypes in one or both of the treatment categories. These results suggest that tolerance and a variety of architectural responses to damage may evolve by both direct and indirect responses to natural selection. While the present study demonstrates the potential importance of cross-treatment genetic correlations in directing the evolution of tolerance traits, such as branch or node production, we did not find any strong evidence of genetic trade-offs in candidate tolerance traits between undamaged and damaged conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Temperature-Stress Resistance and Tolerance along a Latitudinal Cline in North American Arabidopsis lyrata

The study of latitudinal gradients can yield important insights into adaptation to temperature stress. Two strategies are available: resistance by limiting damage, or tolerance by reducing the fitness consequences of damage. Here we studied latitudinal variation in resistance and tolerance to frost and heat and tested the prediction of a trade-off between the two strategies and their costliness. We raised plants of replicate maternal seed families from eight populations of North American Arabidopsis lyrata collected along a latitudinal gradient in climate chambers and exposed them repeatedly to either frost or heat stress, while a set of control plants grew under standard conditions. When control plants reached maximum rosette size, leaf samples were exposed to frost and heat stress, and electrolyte leakage (PEL) was measured and treated as an estimate of resistance. Difference in maximum rosette size between stressed and control plants was used as an estimate of tolerance. Northern populations were more frost resistant, and less heat resistant and less heat tolerant, but—unexpectedly—they were also less frost tolerant. Negative genetic correlations between resistance and tolerance to the same and different thermal stress were generally not significant, indicating only weak trade-offs. However, tolerance to frost was consistently accompanied by small size under control conditions, which may explain the non-adaptive latitudinal pattern for frost tolerance. Our results suggest that adaptation to frost and heat is not constrained by trade-offs between them. But the cost of frost tolerance in terms of plant size reduction may be important for the limits of species distributions and climate niches.     

Genetic Constraints and Selection Acting on Tolerance to Herbivory in the Common Morning Glory Ipomoea purpurea

Tolerance to herbivory minimizes the effects of herbivory on plant fitness. In the presence of herbivores, maximal levels of tolerance may be expected to evolve. In many plant species, however, tolerance is found at an intermediate level. Tolerance may be prevented from evolving to a maximal level by genetic constraints or stabilizing selection. We report on a field study of Ipomoea purpurea, the common morning glory, in which we measured three types of costs that may be associated with tolerance and the pattern of selection acting on tolerance to two types of herbivore damage: apical meristem damage and folivory. We used genetic correlations to test for the presence of three types of costs: a trade-off between tolerance and fitness in the absence of herbivore damage, a trade-off between tolerance and resistance, and genetic covariances among tolerance to different types of damage. We found no evidence that tolerance to apical meristem damage or tolerance to folivory was correlated with resistance, although these two types of tolerance were positively correlated with one another. Tolerance to both types of damage involved costs of lower fitness in the absence of herbivory. Selection acting on tolerance to either type of herbivory was not detected at natural levels of herbivory. Selection is expected to act against tolerance at reduced levels of herbivory and favor tolerance at elevated levels of herbivory. In addition, significant correlational selection gradients indicate that the pattern of selection acting on tolerance depends on values of resistance. Although we found no evidence for stabilizing selection, fluctuating selection resulting from fluctuating herbivore loads may be responsible for maintaining tolerance at an intermediate level.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.     

Multivariate selection and intersexual genetic constraints in a wild bird population

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra‐ and intersex additive genetic (co)variances and sex‐specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex‐specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex‐specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross‐sex genetic correlation = ?0.003, 95% CI = ?0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex‐specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.     

Evolution of increased competitiveness in cows trades off with reduced milk yield,fertility and more masculine morphology

In some species females compete for food, foraging territories, mating, and nesting sites. Competing females can exhibit morphological, physiological, and behavioral adaptations typical of males, which are commonly considered as secondary sexual traits. Competition and the development of traits increasing competitiveness require much energy and may exert adverse effects on fecundity and survival. From an evolutionary perspective, positive selection for increased competitiveness would then result in evolution of reduced values for traits related to fitness such as fecundity and survival. There is recent evidence for such evolutionary trade‐offs involving male competition, but no study has considered competing females so far. Using data from competitions for dominance in cows (Bos taurus), we found negative genetic correlations between traits providing success in competition, that is, fighting ability and fitness traits related to milk production and with fertility (the inverse of parity‐conception interval). Fighting ability also showed low but positive genetic correlations with “masculine” morphological traits, and negative correlations with “feminine” traits. A genetic change in traits over time has occurred due to selection on competitiveness, corresponding to an evolutionary process of “masculinization” counteracting the official selection for milk yield. Similar evolutionary trade‐off between success in competition and fitness components may be present in various species experiencing female competition.     

Using hybrid systems to explore the evolution of tolerance to damage

Hybridization is common and important to the adaptive evolution of plants. Hybridization has resulted in the formation of new species and the introgression of traits between species. This paper discusses the advantages of using hybrid systems to explore the evolution of tolerance to herbivore damage (i.e., the ability to diminish the negative effects of damage on fitness). The major consequence of hybridization likely to make it influential for tolerance evolution is that hybridization generates broad variation in traits that can be selected for or against. In addition to generating greater variation in tolerance to damage and its putative traits (e.g., traits associated with allocation patterns and meristem production), hybridization can generate greater independence among tolerance traits and between tolerance and defense traits. Greater independence may provide a greater ability to discern mechanisms of tolerance, give a greater probability of detecting allocation costs of tolerance, and provide an effective means to evaluate tradeoffs between tolerance and defense. Interspecific hybrid systems can also be used to evaluate the importance of co-adaptation of tolerance traits. Moreover, recombinant hybrids can be used in selection studies focusing on tolerance to damage to discern whether parental combinations of tolerance traits are favored over novel combinations. Research in hybrid systems that investigate the selective importance of tolerance, the patterns of inheritance of tolerance traits, and the genetic architecture of plant species involved can be vital to our evaluation of the adaptive role of tolerance to damage. This revised version was published online in July 2006 with corrections to the Cover Date.     

Tolerance to apical and leaf damage of Raphanus raphanistrum in different competitive regimes

Tolerance to herbivory is an adaptation that promotes regrowth and maintains fitness in plants after herbivore damage. Here, we hypothesized that the effect of competition on tolerance can be different for different genotypes within a species and we tested how tolerance is affected by competitive regime and damage type. We inflicted apical or leaf damage in siblings of 29 families of an annual plant Raphanus raphanistrum (Brassicaceae) grown at high or low competition. There was a negative correlation of family tolerance levels between competition treatments: plant families with high tolerance to apical damage in the low competition treatment had low tolerance to apical damage in the high competition treatment and vice versa. We found no costs of tolerance, in terms of a trade‐off between tolerance to apical and leaf damage or between tolerance and competitive ability, or an allocation cost in terms of reduced fitness of highly tolerant families in the undamaged state. High tolerance bound to a specific competitive regime may entail a cost in terms of low tolerance if competitive regime changes. This could act as a factor maintaining genetic variation for tolerance.     

Effects of pathogen exposure on life‐history variation in the gypsy moth (Lymantria dispar)

Investment in host defences against pathogens may lead to trade‐offs with host fecundity. When such trade‐offs arise from genetic correlations, rates of phenotypic change by natural selection may be affected. However, genetic correlations between host survival and fecundity are rarely quantified. To understand trade‐offs between immune responses to baculovirus exposure and fecundity in the gypsy moth (Lymantria dispar), we estimated genetic correlations between survival probability and traits related to fecundity, such as pupal weight. In addition, we tested whether different virus isolates have different effects on male and female pupal weight. To estimate genetic correlations, we exposed individuals of known relatedness to a single baculovirus isolate. To then evaluate the effect of virus isolate on pupal weight, we exposed a single gypsy moth strain to 16 baculovirus isolates. We found a negative genetic correlation between survival and pupal weight. In addition, virus exposure caused late‐pupating females to be identical in weight to males, whereas unexposed females were 2–3 times as large as unexposed males. Finally, we found that female pupal weight is a quadratic function of host mortality across virus isolates, which is likely due to trade‐offs and compensatory growth processes acting at high and low mortality levels, respectively. Overall, our results suggest that fecundity costs may strongly affect the response to selection for disease resistance. In nature, baculoviruses contribute to the regulation of gypsy moth outbreaks, as pathogens often do in forest‐defoliating insects. We therefore argue that trade‐offs between host life‐history traits may help explain outbreak dynamics.     

Genetic variation in herbivore resistance and tolerance: the role of plant life‐history stage and type of damage

Information of the patterns of genetic variation in plant resistance and tolerance against herbivores and genetic trade‐offs between these two defence strategies is central for our understanding of the evolution of plant defence. We found genetic variation in resistance to two specialist herbivores and in tolerance to artificial damage but not to a specialist leaf herbivore in a long‐lived perennial herb. Seedlings tended to have genetic variation in tolerance to artificial damage. Genetic variation in tolerance of adult plants to artificial damage was not consistent in time. Our results suggest that the level of genetic variation in tolerance and resistance depends on plant life‐history stage, type of damage and timing of estimating the tolerance relative to the occurrence of the damage, which might reflect the pattern of selection imposed by herbivory. Furthermore, we found no trade‐offs between resistance and tolerance, which suggests that the two defence strategies can evolve independently.