Hidden genetic variance contributes to increase the short‐term adaptive potential of selfing populations

Standing genetic variation is considered a major contributor to the adaptive potential of species. The low heritable genetic variation observed in self‐fertilizing populations has led to the hypothesis that species with this mating system would be less likely to adapt. However, a non‐negligible amount of cryptic genetic variation for polygenic traits, accumulated through negative linkage disequilibrium, could prove to be an important source of standing variation in self‐fertilizing species. To test this hypothesis, we simulated populations under stabilizing selection subjected to an environmental change. We demonstrate that, when the mutation rate is high (but realistic), selfing populations are better able to store genetic variance than outcrossing populations through genetic associations, notably due to the reduced effective recombination rate associated with predominant selfing. Following an environmental shift, this diversity can be partially remobilized, which increases the additive variance and adaptive potential of predominantly (but not completely) selfing populations. In such conditions, despite initially lower observed genetic variance, selfing populations adapt as readily as outcrossing ones within a few generations. For low mutation rates, purifying selection impedes the storage of diversity through genetic associations, in which case, as previously predicted, the lower genetic variance of selfing populations results in lower adaptability compared to their outcrossing counterparts. The population size and the mutation rate are the main parameters to consider, as they are the best predictors of the amount of stored diversity in selfing populations. Our results and their impact on our knowledge of adaptation under high selfing rates are discussed.     

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.     

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.     

Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia

High genetic diversity is thought to characterize successful invasive species, as the potential to adapt to new environments is enhanced and inbreeding is reduced. In the last century, guppies, Poecilia reticulata, repeatedly invaded streams in Australia and elsewhere. Quantitative genetic studies of one Australian guppy population have demonstrated high additive genetic variation for autosomal and Y-linked morphological traits. The combination of colonization success, high heritability of morphological traits, and the possibility of multiple introductions to Australia raised the prediction that neutral genetic diversity is high in introduced populations of guppies. In this study we examine genetic diversity at nine microsatellite and one mitochondrial locus for seven Australian populations. We used mtDNA haplotypes from the natural range of guppies and from domesticated varieties to identify source populations. There were a minimum of two introductions, but there was no haplotype diversity within Australian populations, suggesting a founder effect. This was supported by microsatellite markers, as allelic diversity and heterozygosity were severely reduced compared to one wild source population, and evidence of recent bottlenecks was found. Between Australian populations little differentiation of microsatellite allele frequencies was detected, suggesting that population admixture has occurred historically, perhaps due to male-biased gene flow followed by bottlenecks. Thus success of invasion of Australia and high additive genetic variance in Australian guppies are not associated with high levels of diversity at molecular loci. This finding is consistent with the release of additive genetic variation by dominance and epistasis following inbreeding, and with disruptive and negative frequency-dependent selection on fitness traits.     

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.     

Beyond mean allelic effects: A locus at the major color gene MC1R associates also with differing levels of phenotypic and genetic (co)variance for coloration in barn owls

The mean phenotypic effects of a discovered variant help to predict major aspects of the evolution and inheritance of a phenotype. However, differences in the phenotypic variance associated to distinct genotypes are often overlooked despite being suggestive of processes that largely influence phenotypic evolution, such as interactions between the genotypes with the environment or the genetic background. We present empirical evidence for a mutation at the melanocortin‐1‐receptor gene, a major vertebrate coloration gene, affecting phenotypic variance in the barn owl, Tyto alba. The white MC1R allele, which associates with whiter plumage coloration, also associates with a pronounced phenotypic and additive genetic variance for distinct color traits. Contrarily, the rufous allele, associated with a rufous coloration, relates to a lower phenotypic and additive genetic variance, suggesting that this allele may be epistatic over other color loci. Variance differences between genotypes entailed differences in the strength of phenotypic and genetic associations between color traits, suggesting that differences in variance also alter the level of integration between traits. This study highlights that addressing variance differences of genotypes in wild populations provides interesting new insights into the evolutionary mechanisms and the genetic architecture underlying the phenotype.     

Age-dependent genetic variance in a life-history trait in the mute swan

Genetic variance in characters under natural selection in natural populations determines the way those populations respond to that selection. Whether populations show temporal and/or spatial constancy in patterns of genetic variance and covariance is regularly considered, as this will determine whether selection responses are constant over space and time. Much less often considered is whether characters show differing amounts of genetic variance over the life-history of individuals. Such age-specific variation, if present, has important potential consequences for the force of natural selection and for understanding the causes of variation in quantitative characters. Using data from a long-term study of the mute swan Cygnus olor, we report the partitioning of phenotypic variance in timing of breeding (subject to strong natural selection) into component parts over 12 different age classes. We show that the additive genetic variance and heritability of this trait are strongly age-dependent, with higher additive genetic variance present in young and, particularly, old birds, but little evidence of any genetic variance for birds of intermediate ages. These results demonstrate that age can have a very important influence on the components of variation of characters in natural populations, and consequently that separate age classes cannot be assumed to be equivalent, either with respect to their evolutionary potential or response.     

Effect of metal stress on life history divergence and quantitative genetic architecture in a wolf spider

Effects and consequences of stress exposure on life history strategies and quantitative genetic variation in wild populations remain poorly understood. We here study whether long-term exposure to heavy metal pollution may result in alternative life history strategies and alter quantitative genetic properties in natural populations of the wolf spider Pirata piraticus. Offspring originating from a reference and a metal contaminated population and their reciprocal hybrid cross were bred in a half-sib mating scheme and subsequently reared in cadmium contaminated vs. clean environment. Results from this experiment provided evidence for a genetically based reduced growth rate and increased egg size in the contaminated population. Growth rate reduction in response to cadmium contamination was only observed for the reference population. Animal model analysis revealed that heritability for growth rate was large for the reference population under reference conditions, but much lower under metal stressed conditions, caused by a strong decrease in additive genetic variance. Heritability for growth of the metal contaminated population was very low, even under reference conditions. Initial size of the offspring was primarily determined by maternal effects, whereas egg size produced by the offspring was determined by both sire and dam effects, indicating that egg size determination is under control of the female genotype. In conclusion, these results show that metal stress can not only affect life history variation in natural populations, but also decreases the expression as well as the of the amount of genetic variation for particular life history traits.     

The efficiency of close inbreeding to reduce genetic adaptation to captivity

Although ex situ conservation is indispensable for thousands of species, captive breeding is associated with negative genetic changes: loss of genetic variance and genetic adaptation to captivity that is deleterious in the wild. We used quantitative genetic individual-based simulations to model the effect of genetic management on the evolution of a quantitative trait and the associated fitness of wild-born individuals that are brought to captivity. We also examined the feasibility of the breeding strategies under a scenario of a large number of loci subject to deleterious mutations. We compared two breeding strategies: repeated half-sib mating and a method of minimizing mean coancestry (referred to as gc/mc). Our major finding was that half-sib mating is more effective in reducing genetic adaptation to captivity than the gc/mc method. Moreover, half-sib mating retains larger allelic and adaptive genetic variance. Relative to initial standing variation, the additive variance of the quantitative trait increased under half-sib mating during the sojourn in captivity. Although fragmentation into smaller populations improves the efficiency of the gc/mc method, half-sib mating still performs better in the scenarios tested. Half-sib mating shows two caveats that could mitigate its beneficial effects: low heterozygosity and high risk of extinction when populations are of low fecundity and size and one of the following conditions are met: (i) the strength of selection in captivity is comparable with that in the wild, (ii) deleterious mutations are numerous and only slightly deleterious. Experimental validation of half-sib mating is therefore needed for the advancement of captive breeding programs.     

Partitioning of genetic variation across the genome using multimarker methods in a wild bird population

The underlying basis of genetic variation in quantitative traits, in terms of the number of causal variants and the size of their effects, is largely unknown in natural populations. The expectation is that complex quantitative trait variation is attributable to many, possibly interacting, causal variants, whose effects may depend upon the sex, age and the environment in which they are expressed. A recently developed methodology in animal breeding derives a value of relatedness among individuals from high‐density genomic marker data, to estimate additive genetic variance within livestock populations. Here, we adapt and test the effectiveness of these methods to partition genetic variation for complex traits across genomic regions within ecological study populations where individuals have varying degrees of relatedness. We then apply this approach for the first time to a natural population and demonstrate that genetic variation in wing length in the great tit (Parus major) reflects contributions from multiple genomic regions. We show that a polygenic additive mode of gene action best describes the patterns observed, and we find no evidence of dosage compensation for the sex chromosome. Our results suggest that most of the genomic regions that influence wing length have the same effects in both sexes. We found a limited amount of genetic variance in males that is attributed to regions that have no effects in females, which could facilitate the sexual dimorphism observed for this trait. Although this exploratory work focuses on one complex trait, the methodology is generally applicable to any trait for any laboratory or wild population, paving the way for investigating sex‐, age‐ and environment‐specific genetic effects and thus the underlying genetic architecture of phenotype in biological study systems.     

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.     

Mechanisms of constraints: the contributions of selection and genetic variance to the maintenance of cotyledon number in wild radish

The evolutionary mechanisms underlying the maintenance of invariant traits are poorly understood, partly because the lack of variance makes these mechanisms difficult to study. Although the number of cotyledons that plant species produce is highly canalized, populations of plants frequently contain individuals with abnormal cotyledon numbers. In a garden study with 1857 wild radish plants from 75 paternal half-sibling families, 89 (almost 5%) had cotyledon numbers less or greater than two. We found evidence for direct selection on cotyledon number, but no evidence for additive genetic variation for cotyledon number. In spite of the very large sample size, our power to detect variation and selection was hampered by the small number of individuals (10) producing more than two cotyledons. Thus, our results provide support for both a lack of genetic variation and selection as reasons for the current lack of variation in wild radish cotyledon number.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

Potential genetic variance and the domestication of maize

Since Darwin, there has been a long and arduous struggle to understand the source and maintenance of natural genetic variation and its relationship to phenotype. The reason that this task is so difficult is that it requires integration of detailed, and as yet incomplete, knowledge from several biological disciplines, including evolutionary, population, and developmental genetics. In this 'post-genomic' era, it is relatively easy to identify differences in the DNA sequence between individuals. However, the task remains to delineate how this abundant genetic diversity actually contributes to phenotypic diversity. This necessitates tackling the problem of hidden genetic variation. Genetic polymorphisms can be conditionally cryptic, but have the potential to contribute to phenotypic variation in particular genetic backgrounds or under specific environmental conditions. A recent paper by Lauter and Doebley highlights the contribution of hidden genetic variation to traits characterizing the morphological evolution of modern maize from its wild grass-like progenitor teosinte.1 This work is the first to demonstrate hidden variance for selected (agronomically 'adaptive') traits in a well-characterized model for morphological evolution.     

The change in quantitative genetic variation with inbreeding

Inbreeding is known to reduce heterozygosity of neutral genetic markers, but its impact on quantitative genetic variation is debated. Theory predicts a linear decline in additive genetic variance (V(A)) with increasing inbreeding coefficient (F) when loci underlying the trait act additively, but a nonlinear hump-shaped relationship when dominance and epistasis are important. Predictions for heritability (h2) are similar, although the exact shape depends on the value of h2 in the absence of inbreeding. We located 22 published studies in which the level of genetic variation in experimentally inbred populations (measured by V(A) or h2) was compared with that in outbred control populations. For life-history traits, the data strongly supported a nonlinear change in genetic variation with increasing F. V(A) and h2 were, respectively, 244% and 50% higher at F = 0.4 than in outbred populations, and dominance plus epistatic variance together exceeded additive variance by a factor of four. For nonfitness traits the decline was linear and estimates of nonadditive variance were small. These results confirm that population bottlenecks frequently increase V(A) in some traits, and imply that life-history traits are underlain by substantial dominance or epistasis. However, the importance of drift-induced genetic variation in conservation or evolutionary biology is questionable, in part because inbreeding depression usually accompanies inbreeding.     

Evidence for a genetic basis of aging in two wild vertebrate populations

Aging, or senescence, defined as a decline in physiological function with age, has long been a focus of research interest for evolutionary biologists. How has natural selection failed to remove genetic effects responsible for such reduced fitness among older individuals? Current evolutionary theory explains this phenomenon by showing that, as a result of the risk of death from environmental causes that individuals experience, the force of selection inevitably weakens with age. This in turn means that genetic mutations having detrimental effects that are only felt late in life might persist in a population. Although widely accepted, this theory rests on the assumption that there is genetic variation for aging in natural systems, or (equivalently), that genotype-by-age interactions (GxA) occur for fitness. To date, empirical support for this assumption has come almost entirely from laboratory studies on invertebrate systems, most notably Drosophila and C. elegans, whereas tests of genetic variation for aging are largely lacking from natural populations. By using data from two wild mammal populations, we perform quantitative genetic analyses of fitness and provide the first evidence for a genetic basis of senescence to come from a study in the natural environment. We find evidence that genetic differences among individuals cause variation in their rates of aging and that additive genetic variance for fitness increases with age, as predicted by the evolutionary theory of senescence.     

Quantitative genetics of seed size variation inPhlox

Summary Because seed size is often associated with survival and reproduction in plant populations, genetic variation for seed size may be reduced or eliminated by natural selection. To test this hypothesis we assessed genetic sources of variation in seed size in a population ofPhlox drummondii to determine whether genetic differences among seeds influence the size they attain. A diallel cross among 12 plants from a population at Bastrop, Texas, USA allowed us to partition variance in the mass of seeds among several genetic and parental effects. We found no evidence of additive genetic variance or dominance genetic variance for seed mass in the contribution of plants to their offspring. Extranuclear maternal effects accounted for 56% of the variance in seed mass. A small interaction was observed between seed genotype and maternal plant. Results of this study support theory that predicts little genetic variation for traits associated with fitness.     

The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xviii. Clinal and Uniform Genetic Variation over Populations

It has been reported in the previous papers of this series that in the eastern United States and Japan there is a north-to-south cline of additive genetic variance of viability and that the amount of the additive genetic variance in the northern population can be explained by mutation-selection balance. To determine whether or not the difference in the genetic variation in northern and southern populations can be explained by the differences in mutation rate and/or effective population size, numerical calculations were made using population genetic parameters. In addition, the average heterozygosities of the northern and southern populations at ten of 19 polymorphic structural loci surveyed were estimated in relation to the cline of additive genetic variance of viability, and the following findings were obtained. (1) The changes in mutation rate and population size cannot simultaneously explain the difference in additive genetic variance and inbreeding decline between the northern and southern populations. Thus, the operation of some kind of balancing selection, most likely diversifying selection, was suggested to explain the observed excess of additive genetic variance. (2) Estimates of the average heterozygosities of the southern population were not significantly different from those of the northern population. Thus, it was strongly suggested that the excess of additive genetic variance in the southern population cannot be caused by structural loci, but by factors outside the structural loci, and that protein polymorphisms are selectively neutral or nearly neutral.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

Sex-biased genetic component distribution among populations: additive genetic and maternal contributions to phenotypic differences among populations of Chinook salmon

An approach frequently used to demonstrate a genetic basis for population-level phenotypic differences is to employ common garden rearing designs, where observed differences are assumed to be attributable to primarily additive genetic effects. Here, in two common garden experiments, we employed factorial breeding designs between wild and domestic, and among wild populations of Chinook salmon (Oncorhynchus tshawytscha). We measured the contribution of additive (V(A)) and maternal (V(M)) effects to the observed population differences for 17 life history and fitness-related traits. Our results show that, in general, maternal effects contribute more to phenotypic differences among populations than additive genetic effects. These results suggest that maternal effects are important in population phenotypic differentiation and also signify that the inclusion of the maternal source of variation is critical when employing models to test population differences in salmon, such as in local adaptation studies.