Variation in DNA methylation transmissibility,genetic heterogeneity and fecundity‐related traits in natural populations of the perennial herb Helleborus foetidus

Inferences about the role of epigenetics in plant ecology and evolution are mostly based on studies of cultivated or model plants conducted in artificial environments. Insights from natural populations, however, are essential to evaluate the possible consequences of epigenetic processes in biologically realistic scenarios with genetically and phenotypically heterogeneous populations. Here, we explore associations across individuals between DNA methylation transmissibility (proportion of methylation‐sensitive loci whose methylation status persists unchanged after male gametogenesis), genetic characteristics (assessed with AFLP markers), seed size variability (within‐plant seed mass variance), and realized maternal fecundity (number of recently recruited seedlings), in three populations of the perennial herb Helleborus foetidus along a natural ecological gradient in southeastern Spain. Plants (sporophytes) differed in the fidelity with which DNA methylation was transmitted to descendant pollen (gametophytes). This variation in methylation transmissibility was associated with genetic differences. Four AFLP loci were significantly associated with transmissibility and accounted collectively for ~40% of its sample‐wide variance. Within‐plant variance in seed mass was inversely related to individual transmissibility. The number of seedlings recruited by individual plants was significantly associated with transmissibility. The sign of the relationship varied between populations, which points to environment‐specific, divergent phenotypic selection on epigenetic transmissibility. Results support the view that epigenetic transmissibility is itself a phenotypic trait whose evolution may be driven by natural selection, and suggest that in natural populations epigenetic and genetic variation are two intertwined, rather than independent, evolutionary factors.     

Genetic Variance for Body Size in a Natural Population of Drosophila Buzzatii

Previous work has shown thorax length to be under directional selection in the Drosophila buzzatii population of Carboneras. In order to predict the genetic consequences of natural selection, genetic variation for this trait was investigated in two ways. First, narrow sense heritability was estimated in the laboratory F2 generation of a sample of wild flies by means of the offspring-parent regression. A relatively high value, 0.59, was obtained. Because the phenotypic variance of wild flies was 7-9 times that of the flies raised in the laboratory, "natural" heritability may be estimated as one-seventh to one-ninth that value. Second, the contribution of the second and fourth chromosomes, which are polymorphic for paracentric inversions, to the genetic variance of thorax length was estimated in the field and in the laboratory. This was done with the assistance of a simple genetic model which shows that the variance among chromosome arrangements and the variance among karyotypes provide minimum estimates of the chromosome's contribution to the additive and genetic variances of the trait, respectively. In males raised under optimal conditions in the laboratory, the variance among second-chromosome karyotypes accounted for 11.43% of the total phenotypic variance and most of this variance was additive; by contrast, the contribution of the fourth chromosome was nonsignificant. The variance among second-chromosome karyotypes accounted for 1.56-1.78% of the total phenotypic variance in wild males and was nonsignificant in wild females. The variance among fourth chromosome karyotypes accounted for 0.14-3.48% of the total phenotypic variance in wild flies. At both chromosomes, the proportion of additive variance was higher in mating flies than in nonmating flies.     

Quantitative genetic parameters for wild stream‐living brown trout: heritability and parental effects

Adaptability depends on the presence of additive genetic variance for important traits. Yet few estimates of additive genetic variance and heritability are available for wild populations, particularly so for fishes. Here, we estimate heritability of length‐at‐age for wild‐living brown trout (Salmo trutta), based on long‐term mark‐recapture data and pedigree reconstruction based on large‐scale genotyping at 15 microsatellite loci. We also tested for the presence of maternal and paternal effects using a Bayesian version of the Animal model. Heritability varied between 0.16 and 0.31, with reasonable narrow confidence bands, and the total phenotypic variance increased with age. When introducing dam as an additional random effect (accounting for c. 7% of total phenotypic variance), the level of additive genetic variance and heritability decreased (0.12–0.21). Parental size (both for sires and for dams) positively influenced length‐at‐age for juvenile trout – either through direct parental effects or through genotype‐environment correlations. Length‐at‐age is a complex trait reflecting the effects of a number of physiological, behavioural and ecological processes. Our data show that fitness‐related traits such as length‐at‐age can retain high levels of additive genetic variance even when total phenotypic variance is high.     

Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster

Fecundity is usually considered as a trait closely connected to fitness and is expected to exhibit substantial nonadditive genetic variation and inbreeding depression. However, two independent experiments, using populations of different geographical origin, indicate that early fecundity in Drosophila melanogaster behaves as a typical additive trait of low heritability. The first experiment involved artificial selection in inbred and non-inbred lines, all of them started from a common base population previously maintained in the laboratory for about 35 generations. The realized heritability estimate was 0.151 +/- 0.075 and the inbreeding depression was very small and nonsignificant (0.09 +/- 0.09% of the non-inbred mean per 1% increase in inbreeding coefficient). With inbreeding, the observed decrease in the within-line additive genetic variance and the corresponding increase of the between-line variance were very close to their expected values for pure additive gene action. This result is at odds with previous studies showing inbreeding depression and, therefore, directional dominance for the same trait and species. All experiments, however, used laboratory populations, and it is possible that the original genetic architecture of the trait in nature was subsequently altered by the joint action of random drift and adaptation to captivity. Thus, we carried out a second experiment, involving inbreeding without artificial selection in a population recently collected from the wild. In this case we obtained, again, a maximum-likelihood heritability estimate of 0.210 +/- 0.027 and very little nonsignificant inbreeding depression (0.06 +/- 0.12%). The results suggest that, for fitness-component traits, low levels of additive genetic variance are not necessarily associated with large inbreeding depression or high levels of nonadditive genetic variance.     

Resistance to Ergot in Self-incompatible Germplasm Resources of Winter Rye

The poor progress in breeding for resistance to ergot ( Claviceps purpurea [Fr.] Tul.) in rye ( Secale cereale L.) is attributed to the lack of appreciable genotypic variation for this trait. The present study was, therefore, undertaken to evaluate 52 indigenous and exotic genetic resources and 13 open-pollinated cultivars for ergot resistance. These 65 self-incompatible populations were evaluated in four environments with each entry plot surrounded by wheat plots on four sides. Inoculation with a pathogen mixture was done thrice during flowering and harvesting was done early by hand. Resistance traits were ergot incidence and severity. Logit-transformed data were subjected to analyses of variance. The lowest disease severity in any environment was 0.18%, and that was still higher than the official threshold of 0.1% for feed. In the pooled analysis across environments, significant genotypic differences as well as genotype × environment interaction were present. The correlation between ergot severity and pollen shedding was not significant indicating that genotypic differences were not affected by pollen shedding. Broad-sense heritability ( h ² ) estimates were moderate (0.54–0.65). 'Halo', an old German cultivar, and the genetic resources 'Schmidt-Roggen' and 'Dukat', had low ergot severity (Halo having the lowest severity) as well as low disease incidence. The results document a significant, but moderate genotypic variance for ergot resistance among self-incompatible rye that can be exploited to breed ergot-resistant rye.     

Can dominance genetic variance be ignored in evolutionary quantitative genetic analyses of wild populations?

Accurately estimating genetic variance components is important for studying evolution in the wild. Empirical work on domesticated and wild outbred populations suggests that dominance genetic variance represents a substantial part of genetic variance, and theoretical work predicts that ignoring dominance can inflate estimates of additive genetic variance. Whether this issue is pervasive in natural systems is unknown, because we lack estimates of dominance variance in wild populations obtained in situ. Here, we estimate dominance and additive genetic variance, maternal variance, and other sources of nongenetic variance in eight traits measured in over 9000 wild nestlings linked through a genetically resolved pedigree. We find that dominance variance, when estimable, does not statistically differ from zero and represents a modest amount (2-36%) of genetic variance. Simulations show that (1) inferences of all variance components for an average trait are unbiased; (2) the power to detect dominance variance is low; (3) ignoring dominance can mildly inflate additive genetic variance and heritability estimates but such inflation becomes substantial when maternal effects are also ignored. These findings hence suggest that dominance is a small source of phenotypic variance in the wild and highlight the importance of proper model construction for accurately estimating evolutionary potential.     

Genotypic‐specific variance in Caenorhabditis elegans lifetime fecundity

Organisms live in heterogeneous environments, so strategies that maximze fitness in such environments will evolve. Variation in traits is important because it is the raw material on which natural selection acts during evolution. Phenotypic variation is usually thought to be due to genetic variation and/or environmentally induced effects. Therefore, genetically identical individuals in a constant environment should have invariant traits. Clearly, genetically identical individuals do differ phenotypically, usually thought to be due to stochastic processes. It is now becoming clear, especially from studies of unicellular species, that phenotypic variance among genetically identical individuals in a constant environment can be genetically controlled and that therefore, in principle, this can be subject to selection. However, there has been little investigation of these phenomena in multicellular species. Here, we have studied the mean lifetime fecundity (thus a trait likely to be relevant to reproductive success), and variance in lifetime fecundity, in recently‐wild isolates of the model nematode Caenorhabditis elegans. We found that these genotypes differed in their variance in lifetime fecundity: some had high variance in fecundity, others very low variance. We find that this variance in lifetime fecundity was negatively related to the mean lifetime fecundity of the lines, and that the variance of the lines was positively correlated between environments. We suggest that the variance in lifetime fecundity may be a bet‐hedging strategy used by this species.     

Genetic basis of between‐individual and within‐individual variance of docility

Between‐individual variation in phenotypes within a population is the basis of evolution. However, evolutionary and behavioural ecologists have mainly focused on estimating between‐individual variance in mean trait and neglected variation in within‐individual variance, or predictability of a trait. In fact, an important assumption of mixed‐effects models used to estimate between‐individual variance in mean traits is that within‐individual residual variance (predictability) is identical across individuals. Individual heterogeneity in the predictability of behaviours is a potentially important effect but rarely estimated and accounted for. We used 11 389 measures of docility behaviour from 1576 yellow‐bellied marmots (Marmota flaviventris) to estimate between‐individual variation in both mean docility and its predictability. We then implemented a double hierarchical animal model to decompose the variances of both mean trait and predictability into their environmental and genetic components. We found that individuals differed both in their docility and in their predictability of docility with a negative phenotypic covariance. We also found significant genetic variance for both mean docility and its predictability but no genetic covariance between the two. This analysis is one of the first to estimate the genetic basis of both mean trait and within‐individual variance in a wild population. Our results indicate that equal within‐individual variance should not be assumed. We demonstrate the evolutionary importance of the variation in the predictability of docility and illustrate potential bias in models ignoring variation in predictability. We conclude that the variability in the predictability of a trait should not be ignored, and present a coherent approach for its quantification.     

The relationship between parental genetic or phenotypic divergence and progeny variation in the maize nested association mapping population

Appropriate selection of parents for the development of mapping populations is pivotal to maximizing the power of quantitative trait loci detection. Trait genotypic variation within a family is indicative of the family's informativeness for genetic studies. Accurate prediction of the most useful parental combinations within a species would help guide quantitative genetics studies. We tested the reliability of genotypic and phenotypic distance estimators between pairs of maize inbred lines to predict genotypic variation for quantitative traits within families derived from biparental crosses. We developed 25 families composed of ~200 random recombinant inbred lines each from crosses between a common reference parent inbred, B73, and 25 diverse maize inbreds. Parents and families were evaluated for 19 quantitative traits across up to 11 environments. Genetic distances (GDs) among parents were estimated with 44 simple sequence repeat and 2303 single-nucleotide polymorphism markers. GDs among parents had no predictive value for progeny variation, which is most likely due to the choice of neutral markers. In contrast, we observed for about half of the traits measured a positive correlation between phenotypic parental distances and within-family genetic variance estimates. Consequently, the choice of promising segregating populations can be based on selecting phenotypically diverse parents. These results are congruent with models of genetic architecture that posit numerous genes affecting quantitative traits, each segregating for allelic series, with dispersal of allelic effects across diverse genetic material. This architecture, common to many quantitative traits in maize, limits the predictive value of parental genotypic or phenotypic values on progeny variance.     

A MARKER-BASED METHOD FOR INFERENCES ABOUT QUANTITATIVE INHERITANCE IN NATURAL POPULATIONS

A marker-based method for studying quantitative genetic characters in natural populations is presented and evaluated. The method involves regressing quantitative trait similarity on marker-estimated relatedness between individuals. A procedure is first given for estimating the narrow sense heritability and additive genetic correlations among traits, incorporating shared environments. Estimation of the actual variance of relatedness is required for heritability, but not for genetic correlations. The approach is then extended to include isolation by distance of environments, dominance, and shared levels of inbreeding. Investigations of statistical properties show that good estimates do not require great marker polymorphism, but rather require significant variation of actual relatedness; optimal allocation generally favors sampling many individuals at the expense of assaying fewer marker loci; when relatedness declines with physical distance, it is optimal to restrict comparisons to within a certain distance; the power to estimate shared environments and inbreeding effects is reasonable, but estimates of dominance variance may be difficult under certain patterns of relationship; and any linkage of markers to quantitative trait loci does not cause significant problems. This marker-based method makes possible studies with long-lived organisms or with organisms difficult to culture, and opens the possibility that quantitative trait expression in natural environments can be analyzed in an unmanipulative way.     

Heritability and evolvability of fitness and nonfitness traits: Lessons from livestock

Data from natural populations have suggested a disconnection between trait heritability (variance standardized additive genetic variance, V_A) and evolvability (mean standardized V_A) and emphasized the importance of environmental variation as a determinant of trait heritability but not evolvability. However, these inferences are based on heterogeneous and often small datasets across species from different environments. We surveyed the relationship between evolvability and heritability in >100 traits in farmed cattle, taking advantage of large sample sizes and consistent genetic approaches. Heritability and evolvability estimates were positively correlated (r = 0.37/0.54 on untransformed/log scales) reflecting a substantial impact of V_A on both measures. Furthermore, heritabilities and residual variances were uncorrelated. The differences between this and previously described patterns may reflect lower environmental variation experienced in farmed systems, but also low and heterogeneous quality of data from natural populations. Similar to studies on wild populations, heritabilities for life‐history and behavioral traits were lower than for other traits. Traits having extremely low heritabilities and evolvabilities (17% of the studied traits) were almost exclusively life‐history or behavioral traits, suggesting that evolutionary constraints stemming from lack of genetic variability are likely to be most common for classical “fitness” (cf. life‐history) rather than for “nonfitness” (cf. morphological) traits.     

Shared spatial effects on quantitative genetic parameters: accounting for spatial autocorrelation and home range overlap reduces estimates of heritability in wild red deer

Social structure, limited dispersal, and spatial heterogeneity in resources are ubiquitous in wild vertebrate populations. As a result, relatives share environments as well as genes, and environmental and genetic sources of similarity between individuals are potentially confounded. Quantitative genetic studies in the wild therefore typically account for easily captured shared environmental effects (e.g., parent, nest, or region). Fine-scale spatial effects are likely to be just as important in wild vertebrates, but have been largely ignored. We used data from wild red deer to build "animal models" to estimate additive genetic variance and heritability in four female traits (spring and rut home range size, offspring birth weight, and lifetime breeding success). We then, separately, incorporated spatial autocorrelation and a matrix of home range overlap into these models to estimate the effect of location or shared habitat on phenotypic variation. These terms explained a substantial amount of variation in all traits and their inclusion resulted in reductions in heritability estimates, up to an order of magnitude up for home range size. Our results highlight the potential of multiple covariance matrices to dissect environmental, social, and genetic contributions to phenotypic variation, and the importance of considering fine-scale spatial processes in quantitative genetic studies.     

Maintenance of genetic variation in quantitative traits of a woodland rodent during generations of captive breeding

Breeding programs to conserve diversity are predicated on the assumption that genetic variation in adaptively important traits will be lost in parallel to the loss of variation at neutral loci. To test this assumption, we monitored quantitative traits across 18 generations of Peromyscus leucopus mice propagated with protocols that mirror breeding programs for threatened species. Ears, hind feet, and tails became shorter, but changes were reversible by outcrossing and therefore were due to accumulated inbreeding. Heritability of ear length decreased, because of an increase in phenotypic variance rather than the expected decrease in additive genetic variance. Additive genetic variance in hind foot length increased. This trait initially had low heritability but large dominance or common environmental variance contributing to resemblance among full-sibs. The increase in the additive component indicates that there was conversion of interaction variances to additive variance. For no trait did additive genetic variation decrease significantly across generations. These findings indicate that the restructuring of genetic variance that occurs with genetic drift and novel selection in captivity can prevent or delay the loss of phenotypic and heritable variation, providing variation on which selection can act to adapt populations to captivity and perhaps later to readapt to more natural habitats after release. Therefore, the importance of minimizing loss of gene diversity from conservation breeding programs for threatened wildlife species might lie in preventing immediate reduction in individual fitness due to inbreeding and protecting allelic diversity for long-term evolutionary change, more so than in protecting variation in quantitative traits for rapid re-adaptation to wild environments.     

A QUANTITATIVE-GENETIC MODEL FOR SELECTION ON DEVELOPMENTAL NOISE

We propose a simple model for analyzing the effects of microenvironmental variation in quantitative genetics. Our model assumes that the sensitivity of the phenotype to fluctuations in microenvironment has a genetic basis and allows for genetic correlation between trait value and microenvironmental sensitivity. We analyze the effects of short-term stabilizing and directional selection on the genotypic and microenvironmental components of phenotypic variance. Our model predicts that stabilizing selection on a quantitative trait increases developmental canalization. We show that stabilizing selection can result in an increase in the heritability. Our findings may provide an explanation for the results of selection experiments in which artificial stabilizing selection did not change the heritability coefficient or increased it.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

Mendelian Factors Underlying Quantitative Traits in Tomato: Comparison across Species, Generations, and Environments

As part of ongoing studies regarding the genetic basis of quantitative variation in phenotype, we have determined the chromosomal locations of quantitative trait loci (QTLs) affecting fruit size, soluble solids concentration, and pH, in a cross between the domestic tomato (Lycopersicon esculentum Mill.) and a closely-related wild species, L. cheesmanii. Using a RFLP map of the tomato genome, we compared the inheritance patterns of polymorphisms in 350 F2 individuals with phenotypes scored in three different ways: (1) from the F2 progeny themselves, grown near Davis, California; (2) from F3 families obtained by selfing each F2 individual, grown near Gilroy, California (F3-CA); and (3) from equivalent F3 families grown near Rehovot, Israel (F3-IS). Maximum likelihood methods were used to estimate the approximate chromosomal locations, phenotypic effects (both additive effects and dominance deviations), and gene action of QTLs underlying phenotypic variation in each of these three environments. A total of 29 putative QTLs were detected in the three environments. These QTLs were distributed over 11 of the 12 chromosomes, accounted for 4.7-42.0% of the phenotypic variance in a trait, and showed different types of gene action. Among these 29 QTLs, 4 were detected in all three environments, 10 in two environments, and 15 in only a single environment. The two California environments were most similar, sharing 11/25 (44%) QTLs, while the Israel environment was quite different, sharing 7/20 (35%) and 5/26 (19%) QTLs with the respective California environments. One major goal of QTL mapping is to predict, with maximum accuracy, which individuals will produce progeny showing particular phenotypes. Traditionally, the phenotype of an individual alone has been used to predict the phenotype of its progeny. Our results suggested that, for a trait with low heritability (soluble solids), the phenotype of F3 progeny could be predicted more accurately from the genotype of the F2 parent at QTLs than from the phenotype of the F2 individual. For a trait with intermediate heritability (fruit pH), QTL genotype and observed phenotype were about equally effective at predicting progeny phenotype. For a trait with high heritability (mass per fruit), knowing the QTL genotype of an individual added little if any predictive value, to simply knowing the phenotype. The QTLs mapped in the L. esculentum X L. cheesmanii F2 appear to be at similar locations to many of those mapped in a previous cross with a different wild tomato (L. chmielewskii).(ABSTRACT TRUNCATED AT 400 WORDS)     

Heritability of resting metabolic rate in a wild population of blue tits

We report the first study with the aim to estimate heritability in a wild population, a nest box breeding population of blue tits. We estimated heritability as well as genetic and phenotypic correlations of resting metabolic rate (RMR), body mass and tarsus length with an animal model based on data from a split cross‐fostering experiment with brood size manipulations. RMR and body mass, but not tarsus length, showed significant levels of explained variation but for different underlying reasons. In body mass, the contribution to the explained variation is mainly because of a strong brood effect, while in RMR it is mainly because of a high heritability. The additive variance in RMR was significant and the heritability was estimated to 0.59. The estimates of heritability of body mass (0.08) and tarsus length (0.00) were both low and based on nonsignificant additive variances. Thus, given the low heritability (and additive variances) in body mass and tarsus length the potential for direct selection on RMR independent of the two traits is high in this population. However, the strong phenotypic correlation between RMR and mass (0.643 ± 0.079) was partly accounted for by a potentially strong, although highly uncertain, genetic correlation (1.178 ± 0.456) between the two traits. This indicates that the additive variance of body mass, although low, might still somewhat constrain the independent evolvability of RMR.     

Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach

Males of the noctuid moths, Heliothis virescens and H. subflexa locate mates based on species-specific responses to female-emitted pheromones that are composed of distinct blends of volatile compounds. We conducted genetic crosses between these two species and used AFLP marker-based mapping of backcross families (H. subflexa direction) to determine which of the 30 autosomes in these moths contained quantitative trait loci (QTL) controlling the proportion of specific chemical components in the pheromone blends. Presence/absence of single H. virescens chromosomes accounted for 7-34% of the phenotypic variation among backcross females in seven pheromone components. For a set of three similar 16-carbon acetates, two H. virescens chromosomes interacted in determining their relative amounts within the pheromone gland and together accounted for 53% of the phenotypic variance. Our results are discussed relative to theories about population genetic processes and biochemical mechanisms involved in the evolution of new sexual communication systems.     

Epigenetic variation predicts regional and local intraspecific functional diversity in a perennial herb

The ecological significance of epigenetic variation has been generally inferred from studies on model plants under artificial conditions, but the importance of epigenetic differences between individuals as a source of intraspecific diversity in natural plant populations remains essentially unknown. This study investigates the relationship between epigenetic variation and functional plant diversity by conducting epigenetic (methylation‐sensitive amplified fragment length polymorphisms, MSAP) and genetic (amplified fragment length polymorphisms, AFLP) marker–trait association analyses for 20 whole‐plant, leaf and regenerative functional traits in a large sample of wild‐growing plants of the perennial herb Helleborus foetidus from ten sampling sites in south‐eastern Spain. Plants differed widely in functional characteristics, and exhibited greater epigenetic than genetic diversity, as shown by per cent polymorphism of MSAP fragments (92%) or markers (69%) greatly exceeding that for AFLP ones (41%). After controlling for genetic structuring and possible cryptic relatedness, every functional trait considered exhibited a significant association with at least one AFLP or MSAP marker. A total of 27 MSAP (13.0% of total) and 12 AFLP (4.4%) markers were involved in significant associations, which explained on average 8.2% and 8.0% of trait variance, respectively. Individual MSAP markers were more likely to be associated with functional traits than AFLP markers. Between‐site differences in multivariate functional diversity were directly related to variation in multilocus epigenetic diversity after multilocus genetic diversity was statistically accounted for. Results suggest that epigenetic variation can be an important source of intraspecific functional diversity in H. foetidus, possibly endowing this species with the capacity to exploit a broad range of ecological conditions despite its modest genetic diversity.