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.     

Heritability of flight and resting metabolic rates in the Glanville fritillary butterfly

Dispersal capacity is a key life‐history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates (RMRs) in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate (FMR) is known to correlate strongly with dispersal rate. We modelled a two‐generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that FMR is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus, FMR has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context dependent, as in stressful thermal conditions, environmentally induced variation dominated over additive genetic effects. There was no heritability in RMR, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal‐related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats.     

Multilevel selection 1: Quantitative genetics of inheritance and response to selection

Interaction among individuals is universal, both in animals and in plants, and substantially affects evolution of natural populations and responses to artificial selection in agriculture. Although quantitative genetics has successfully been applied to many traits, it does not provide a general theory accounting for interaction among individuals and selection acting on multiple levels. Consequently, current quantitative genetic theory fails to explain why some traits do not respond to selection among individuals, but respond greatly to selection among groups. Understanding the full impacts of heritable interactions on the outcomes of selection requires a quantitative genetic framework including all levels of selection and relatedness. Here we present such a framework and provide expressions for the response to selection. Results show that interaction among individuals may create substantial heritable variation, which is hidden to classical analyses. Selection acting on higher levels of organization captures this hidden variation and therefore always yields positive response, whereas individual selection may yield response in the opposite direction. Our work provides testable predictions of response to multilevel selection and reduces to classical theory in the absence of interaction. Statistical methodology provided elsewhere enables empirical application of our work to both natural and domestic populations.     

Genetic variance for behavioural ‘predictability’ of stress response

Genetic factors underpinning phenotypic variation are required if natural selection is to result in adaptive evolution. However, evolutionary and behavioural ecologists typically focus on variation among individuals in their average trait values and seek to characterize genetic contributions to this. As a result, less attention has been paid to if and how genes could contribute towards within‐individual variance or trait ‘predictability’. In fact, phenotypic ‘predictability’ can vary among individuals, and emerging evidence from livestock genetics suggests this can be due to genetic factors. Here, we test this empirically using repeated measures of a behavioural stress response trait in a pedigreed population of wild‐type guppies. We ask (a) whether individuals differ in behavioural predictability and (b) whether this variation is heritable and so evolvable under selection. Using statistical methodology from the field of quantitative genetics, we find support for both hypotheses and also show evidence of a genetic correlation structure between the behavioural trait mean and individual predictability. We show that investigating sources of variability in trait predictability is statistically tractable and can yield useful biological interpretation. We conclude that, if widespread, genetic variance for ‘predictability’ will have major implications for the evolutionary causes and consequences of phenotypic variation.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. III. PHENOTYPIC PLASTICITY AND THE MAINTENANCE OF GENETIC VARIATION

Cheilostome bryozoan species show long-term morphologic stasis, implying stabilizing selection sustained for millions of years, but nevertheless retain significant heritable variation in traits of skeletal morphology. The possible role of within-genotype (within-colony) phenotypic variability in preserving genetic diversity was analyzed using breeding data for two species of Stylopoma from sites along 110 km of the Caribbean coast of Panama. Variation among zooids within colonies accounts for nearly two-thirds of the phenotypic variance on average, increases with environmental heterogeneity, and includes significant genotype-environment interaction. Thus, within-colony variability apparently represents phenotypic plasticity, at least some of which is heritable, rather than random “developmental noise.” Almost all of the among-colonies component of phenotypic variance is accounted for by additive genetic differences in trait means, suggesting that within-colony plasticity includes virtually all of the environmental component of phenotypic variance in these populations of Stylopoma. Thus, heritable within-colony plasticity could play a significant part in maintaining genetic diversity in cheilostomes, but it is also possible that rates of polygenic mutation alone are sufficient to balance the effects of selection.     

Maternal genetic effects set the potential for evolution in a free-living vertebrate population

Heritable maternal effects have important consequences for the evolutionary dynamics of phenotypic traits under selection, but have only rarely been tested for or quantified in evolutionary studies. Here we estimate maternal effects on early-life traits in a feral population of Soay sheep (Ovis aries) from St Kilda, Scotland. We then partition the maternal effects into genetic and environmental components to obtain the first direct estimates of maternal genetic effects in a free-living population, and furthermore test for covariance between direct and maternal genetic effects. Using an animal model approach, direct heritabilities (h2) were low but maternal genetic effects (m2) represented a relatively large proportion of the total phenotypic variance for each trait (birth weight m2=0.119, birth date m2=0.197, natal litter size m2=0.211). A negative correlation between direct and maternal genetic effects was estimated for each trait, but was only statistically significant for natal litter size (ram= -0.714). Total heritabilities (incorporating variance from heritable maternal effects and the direct-maternal genetic covariance) were significant for birth weight and birth date but not for natal litter size. Inadequately specified models greatly overestimated additive genetic variance and hence direct h2 (by a factor of up to 6.45 in the case of birth date). We conclude that failure to model heritable maternal variance can result in over- or under-estimation of the potential for traits to respond to selection, and advocate an increased effort to explicitly measure maternal genetic effects in evolutionary 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.     

Field heritability of a plant adaptation to fire in heterogeneous landscapes

The strong association observed between fire regimes and variation in plant adaptations to fire suggests a rapid response to fire as an agent of selection. It also suggests that fire‐related traits are heritable, a precondition for evolutionary change. One example is serotiny, the accumulation of seeds in unopened fruits or cones until the next fire, an important strategy for plant population persistence in fire‐prone ecosystems. Here, we evaluate the potential of this trait to respond to natural selection in its natural setting. For this, we use a SNP marker approach to estimate genetic variance and heritability of serotiny directly in the field for two Mediterranean pine species. Study populations were large and heterogeneous in climatic conditions and fire regime. We first estimated the realized relatedness among trees from genotypes, and then partitioned the phenotypic variance in serotiny using Bayesian animal models that incorporated environmental predictors. As expected, field heritability was smaller (around 0.10 for both species) than previous estimates under common garden conditions (0.20). An estimate on a subset of stands with more homogeneous environmental conditions was not different from that in the complete set of stands, suggesting that our models correctly captured the environmental variation at the spatial scale of the study. Our results highlight the importance of measuring quantitative genetic parameters in natural populations, where environmental heterogeneity is a critical aspect. The heritability of serotiny, although not high, combined with high phenotypic variance within populations, confirms the potential of this fire‐related trait for evolutionary change in the wild.     

Small‐scale spatial variation in evolvability for life‐history traits in the storm petrel

The evolutionary potential in the timing of recruitment and reproduction may be crucial for the ability of populations to buffer against environmental changes, allowing them to avoid unfavourable breeding conditions. The evolution of a trait in a local population is determined by its heritability and selection. In the present study, we performed pedigree‐based quantitative genetic analyses for two life‐history traits (recruiting age and laying date) using population data of the storm petrel over an 18‐year period in two adjacent breeding colonies (only 150 m apart) that share the same environmental conditions. In both traits, natal colony effect was the main source of the phenotypic variation among individuals, and cohort variance for recruitment age and additive genetic variance for laying date were natal colony‐specific. We found significant heritability only in laying date and, more specifically, only in birds born in one of the colonies. The difference in genetic variance between the colonies was statistically significant. Interestingly, selection on earlier breeding birds was detected only in the colony in which heritable variation in laying date was found. Therefore, local evolvability for a life‐history trait may vary within a unexpectedly small spatial scale, through the diversifying natural selection and insulating gene flow. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 439–446.     

Age-specific genetic and maternal effects in fecundity of preindustrial Finnish women

A population's potential for evolutionary change depends on the amount of genetic variability expressed in traits under selection. Studies attempting to measure this variability typically do so over the life span of individuals, but theory suggests that the amount of additive genetic variance can change during the course of individuals' lives. Here we use pedigree data from historical Finns and a quantitative genetic framework to investigate how female fecundity, throughout an individual's reproductive life, is influenced by "maternal" versus additive genetic effects. We show that although maternal effects explain variation in female fecundity early in life, these effects wane with female age. Moreover, this decline in maternal effects is associated with a concomitant increase in additive genetic variance with age. Our results thus highlight that single over-lifetime estimates of trait heritability may give a misleading view of a trait's potential to respond to changing selection pressures.     

Direct and indirect responses to selection on pollen size in Brassica rapa L.

Pollen size varies little within angiosperm species, but differs extensively between species, suggesting the action of strong selection. Nevertheless, the potential for genetic responses of pollen size to selection, as determined by additive genetic variance and genetic correlations with other floral traits, has received little attention. To assess this potential, we subjected Brassica rapa to artificial selection for large and small pollen during three generations. This selection caused significant divergence in pollen diameter, with additive genetic effects accounting for over 30% of the observed phenotypic variation in pollen size. Such heritable genetic variation suggests that natural selection could effect evolutionary change in this trait. Selection on pollen size also elicited correlated responses in pollen number (–), flower size (+), style length (+), and ovule number (+), suggesting that pollen size cannot evolve independently. The correlated responses of pollen number, flower size and ovule number probably reflect the genetically determined and physically constrained pattern of resource allocation in B. rapa. In contrast, the positive correlation between pollen size and style length may represent a widespread gametic‐phase disequilibrium in angiosperms that arises from nonrandom fertilization success of large pollen in pistils with long styles.     

Genes,development, and evolvability in primate evolution

Development is the process whereby a fertilized cell becomes a mature individual. In metazoans, this complex process involves the differentiation of somatic cells into committed cell and tissue types; the organization and migration of cells, tissues, and anatomical structures relative to one another; and growth. 1 Development matters to evolution in two ways. First, development carries out heritable genetic instructions contained in zygotes to produce functioning yet phenotypically varied individuals. At the population level, this variation in form and function among individuals provides the “raw material” for evolution. Second, the mechanisms of development influence the magnitude, direction, and interdependence of heritable phenotypic variation among traits. Together with phenomena such as genetic drift, organismal development determines the raw material available to selection and thus influences the rate and direction of phenotypic evolution. 2 , 3     

Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population

Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.     

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.     

Alternative developmental pathways and the propensity to migrate: a case study in the Atlantic salmon

Migratory behaviour with its associated phenotypic changes is generally viewed as an adaptive strategy because it incurs survival or reproductive advantages to migrants. The development of a migrant phenotype is believed to be controlled by threshold mechanisms, where individuals emigrate only after surpassing a particular body size but delay migration if below. For such a strategy to respond to natural selection, part of the phenotypic variance in the propensity to migrate must be explained by variation in additive genetic effects. Here, we use data gathered in the field and from a common rearing experiment to test for a genetic basis associated with seaward migration in Atlantic salmon (Salmo salar L.). We document a high heritability of the liability trait underlying the propensity to emigrate in juvenile salmon, and significant differences between offspring grouped according to their sires in body-size threshold values above which emigration takes place. The presence of additive genetic variance in both the liability and thresholds makes the onset of migration a process sensitive to selection and may therefore constitute an important explanatory mechanism for the interpopulation differences in the size at seaward migration observed in this species.     

An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population

Glucocorticoid hormones (CORT) are predicted to promote adaptation to variable environments, yet little is known about the potential for CORT secretion patterns to respond to selection in free-living populations. We assessed the heritable variation underlying differences in hormonal phenotypes using a cross-foster experimental design with nestling North American barn swallows (Hirundo rustica erythrogaster). Using a bivariate animal model, we partitioned variance in baseline and stress-induced CORT concentrations into their additive genetic and rearing environment components and estimated their genetic correlation. Both baseline and stress-induced CORT were heritable with heritability of 0.152 and 0.343, respectively. We found that the variation in baseline CORT was best explained by rearing environment, whereas the variation in stress-induced CORT was contributed to by a combination of genetic and environmental factors. Further, we did not detect a genetic correlation between these two hormonal traits. Although rearing environment appears to play an important role in the secretion of both types of CORT, our results suggest that stress-induced CORT levels are underlain by greater additive genetic variance compared with baseline CORT levels. Accordingly, we infer that the glucocorticoid response to stress has a greater potential for evolutionary change in response to selection compared with baseline glucocorticoid secretion patterns.     

Multilevel selection 2: Estimating the genetic parameters determining inheritance and response to selection

Interactions among individuals are universal, both in animals and in plants and in natural as well as domestic populations. Understanding the consequences of these interactions for the evolution of populations by either natural or artificial selection requires knowledge of the heritable components underlying them. Here we present statistical methodology to estimate the genetic parameters determining response to multilevel selection of traits affected by interactions among individuals in general populations. We apply these methods to obtain estimates of genetic parameters for survival days in a population of layer chickens with high mortality due to pecking behavior. We find that heritable variation is threefold greater than that obtained from classical analyses, meaning that two-thirds of the full heritable variation is hidden to classical analysis due to social interactions. As a consequence, predicted responses to multilevel selection applied to this population are threefold greater than classical predictions. This work, combined with the quantitative genetic theory for response to multilevel selection presented in an accompanying article in this issue, enables the design of selection programs to effectively reduce competitive interactions in livestock and plants and the prediction of the effects of social interactions on evolution in natural populations undergoing multilevel selection.     

Epialleles via DNA methylation: consequences for plant evolution

In plants, naturally occurring methylation of genes can affect the level of gene expression. Variation among individuals in the degree of methylation of a gene, termed epialleles, produces novel phenotypes that are heritable across generations. To date, ecologically important genes with methylated epialleles have been found to affect floral shape, vegetative and seed pigmentation, pathogen resistance and development in plants. Currently, the extent to which epiallelic variation is an important common contributor to phenotypic variation in natural plant populations and its fitness consequences are not known. Because epiallele phenotypes can have identical underlying DNA sequences, response to selection on these phenotypes is likely to differ from expectations based on traditional models of microevolution. Research is needed to understand the role of epialleles in natural plant populations. Recent advances in molecular genetic techniques could enable population biologists to screen for epiallelic variants within plant populations and disentangle epigenetic from more standard genetic sources of phenotypic variance, such as additive genetic variance, dominance variance, epistasis and maternal genetic effects.     

The contribution of social effects to heritable variation in finishing traits of domestic pigs (Sus scrofa)

Social interactions among individuals are ubiquitous both in animals and in plants, and in natural as well as domestic populations. These interactions affect both the direction and the magnitude of responses to selection and are a key factor in evolutionary success of species and in the design of breeding schemes in agriculture. At present, however, very little is known of the contribution of social effects to heritable variance in trait values. Here we present estimates of the direct and social genetic variance in growth rate, feed intake, back fat thickness, and muscle depth in a population of 14,032 domestic pigs with known pedigree. Results show that social effects contribute the vast majority of heritable variance in growth rate and feed intake in this population. Total heritable variance expressed relative to phenotypic variance was 71% for growth rate and 70% for feed intake. These values clearly exceed the usual range of heritability for those traits. Back fat thickness and muscle depth showed no heritable variance due to social effects. Our results suggest that genetic improvement in agriculture can be substantially advanced by redirecting breeding schemes, so as to capture heritable variance due to social effects.     

Environmental coupling of selection and heritability limits evolution

There has recently been great interest in applying theoretical quantitative genetic models to empirical studies of evolution in wild populations. However, while classical models assume environmental constancy, most natural populations exist in variable environments. Here, we applied a novel analytical technique to a long-term study of birthweight in wild sheep and examined, for the first time, how variation in environmental quality simultaneously influences the strength of natural selection and the genetic basis of trait variability. In addition to demonstrating that selection and genetic variance vary dramatically across environments, our results show that environmental heterogeneity induces a negative correlation between these two parameters. Harsh environmental conditions were associated with strong selection for increased birthweight but low genetic variance, and vice versa. Consequently, the potential for microevolution in this population is constrained by either a lack of heritable variation (in poor environments) or by a reduced strength of selection (in good environments). More generally, environmental dependence of this nature may act to limit rates of evolution, maintain genetic variance, and favour phenotypic stasis in many natural systems. Assumptions of environmental constancy are likely to be violated in natural systems, and failure to acknowledge this may generate highly misleading expectations for phenotypic microevolution.