COMPARING STRENGTHS OF DIRECTIONAL SELECTION: HOW STRONG IS STRONG?

The fundamental equation in evolutionary quantitative genetics, the Lande equation, describes the response to directional selection as a product of the additive genetic variance and the selection gradient of trait value on relative fitness. Comparisons of both genetic variances and selection gradients across traits or populations require standardization, as both are scale dependent. The Lande equation can be standardized in two ways. Standardizing by the variance of the selected trait yields the response in units of standard deviation as the product of the heritability and the variance-standardized selection gradient. This standardization conflates selection and variation because the phenotypic variance is a function of the genetic variance. Alternatively, one can standardize the Lande equation using the trait mean, yielding the proportional response to selection as the product of the squared coefficient of additive genetic variance and the mean-standardized selection gradient. Mean-standardized selection gradients are particularly useful for summarizing the strength of selection because the mean-standardized gradient for fitness itself is one, a convenient benchmark for strong selection. We review published estimates of directional selection in natural populations using mean-standardized selection gradients. Only 38 published studies provided all the necessary information for calculation of mean-standardized gradients. The median absolute value of multivariate mean-standardized gradients shows that selection is on average 54% as strong as selection on fitness. Correcting for the upward bias introduced by taking absolute values lowers the median to 31%, still very strong selection. Such large estimates clearly cannot be representative of selection on all traits. Some possible sources of overestimation of the strength of selection include confounding environmental and genotypic effects on fitness, the use of fitness components as proxies for fitness, and biases in publication or choice of traits to study.     

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-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.     

The effect of trait type and strength of selection on heritability and evolvability in an island bird population

The heritability (h²) of fitness traits is often low. Although this has been attributed to directional selection having eroded genetic variation in direct proportion to the strength of selection, heritability does not necessarily reflect a trait's additive genetic variance and evolutionary potential (“evolvability”). Recent studies suggest that the low h² of fitness traits in wild populations is caused not by a paucity of additive genetic variance (V_A) but by greater environmental or nonadditive genetic variance (V_R). We examined the relationship between h² and variance‐standardized selection intensities (i or β_σ), and between evolvability (I_A:V_A divided by squared phenotypic trait mean) and mean‐standardized selection gradients (β_μ). Using 24 years of data from an island population of Savannah sparrows, we show that, across diverse traits, h² declines with the strength of selection, whereas I_A and I_R (V_R divided by squared trait mean) are independent of the strength of selection. Within trait types (morphological, reproductive, life‐history), h², I_A, and I_R are all independent of the strength of selection. This indicates that certain traits have low heritability because of increased residual variance due to the age at which they are expressed or the multiple factors influencing their expression, rather than their association with fitness.     

How does selfing affect the genetic variance of quantitative traits? An updated meta‐analysis on empirical results in angiosperm species

Most theoretical works predict that selfing should reduce the level of additive genetic variance available for quantitative traits within natural populations. Despite a growing number of quantitative genetic studies undertaken during the last two decades, this prediction is still not well supported empirically. To resolve this issue and confirm or reject theoretical predictions, we reviewed quantitative trait heritability estimates from natural plant populations with different rates of self‐fertilization and carried out a meta‐analysis. In accordance with models of polygenic traits under stabilizing selection, we found that the fraction of additive genetic variance is negatively correlated with the selfing rate. Although the mating system explains a moderate fraction of the variance, the mean reduction of narrow‐sense heritability values between strictly allogamous and predominantly selfing populations is strong, around 60%. Because some nonadditive components of genetic variance become selectable under inbreeding, we determine whether self‐fertilization affects the relative contribution of these components to genetic variance by comparing narrow‐sense heritability estimates from outcrossing populations with broad‐sense heritability estimated in autogamous populations. Results suggest that these nonadditive components of variance may restore some genetic variance in predominantly selfing populations; it remains, however, uncertain how these nonadditive components will contribute to adaptation.     

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.     

Assortative mating and gene flow generate clinal phenological variation in trees

ABSTRACT: BACKGROUND: On-going climate change is shifting the timing of bud burst (TBB) of broad leaf and conifer trees in temperate areas, raising concerns about the abilities of natural populations to respond to these shifts. The level of expected evolutionary change depends on the level and distribution of genetic variation of TBB. While numerous experimental studies have highlighted the role of divergent selection in promoting clinal TBB differentiation, we explored whether the observed patterns of variation could be generated by the joint effects of assortative mating for TBB and gene flow among natural populations. We tested this hypothesis using an in silico approach based on quantitative genetic models. RESULTS: Our simulations showed that genetic clines can develop even without divergent selection. Assortative mating in association with environmental gradients substantially shifted the mean genetic values of populations. Owing to assortative mating, immigrant alleles were screened for proximal or distant populations depending on the strength of the environmental cline. Furthermore, we confirmed that assortative mating increases the additive genetic variance within populations. However, we observed also a rapid decline of the additive genetic variance caused by restricted gene flow between neighboring populations resulting from preferential matings between phenologically-matching phenotypes. CONCLUSIONS: We provided evidence that the patterns of genetic variation of phenological traits observed in forest trees can be generated solely by the effects of assortative mating and gene flow. We anticipate that predicted temperature increases due to climate change will further enhance genetic differentiation across the landscape. These trends are likely to be reinforced or counteracted by natural selection if phenological traits are correlated to fitness.     

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.     

Prediction of breeding values and selection responses with genetic heterogeneity of environmental variance

There is empirical evidence that genotypes differ not only in mean, but also in environmental variance of the traits they affect. Genetic heterogeneity of environmental variance may indicate genetic differences in environmental sensitivity. The aim of this study was to develop a general framework for prediction of breeding values and selection responses in mean and environmental variance with genetic heterogeneity of environmental variance. Both means and environmental variances were treated as heritable traits. Breeding values and selection responses were predicted with little bias using linear, quadratic, and cubic regression on individual phenotype or using linear regression on the mean and within-family variance of a group of relatives. A measure of heritability was proposed for environmental variance to standardize results in the literature and to facilitate comparisons to "conventional" traits. Genetic heterogeneity of environmental variance can be considered as a trait with a low heritability. Although a large amount of information is necessary to accurately estimate breeding values for environmental variance, response in environmental variance can be substantial, even with mass selection. The methods developed allow use of the well-known selection index framework to evaluate breeding strategies and effects of natural selection that simultaneously change the mean and the variance.     

Bias in the prediction of genetic gain due to mass and half-sib selection in random mating populations

The prediction of gains from selection allows the comparison of breeding methods and selection strategies, although these estimates may be biased. The objective of this study was to investigate the extent of such bias in predicting genetic gain. For this, we simulated 10 cycles of a hypothetical breeding program that involved seven traits, three population classes, three experimental conditions and two breeding methods (mass and half-sib selection). Each combination of trait, population, heritability, method and cycle was repeated 10 times. The predicted gains were biased, even when the genetic parameters were estimated without error. Gain from selection in both genders is twice the gain from selection in a single gender only in the absence of dominance. The use of genotypic variance or broad sense heritability in the predictions represented an additional source of bias. Predictions based on additive variance and narrow sense heritability were equivalent, as were predictions based on genotypic variance and broad sense heritability. The predictions based on mass and family selection were suitable for comparing selection strategies, whereas those based on selection within progenies showed the largest bias and lower association with the realized gain.     

Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population

Body size is an important determinant of fitness in many organisms. While size will typically change over the lifetime of an individual, heritable components of phenotypic variance may also show ontogenetic variation. We estimated genetic (additive and maternal) and environmental covariance structures for a size trait (June weight) measured over the first 5 years of life in a natural population of bighorn sheep Ovis canadensis. We also assessed the utility of random regression models for estimating these structures. Additive genetic variance was found for June weight, with heritability increasing over ontogeny because of declining environmental variance. This pattern, mirrored at the phenotypic level, likely reflects viability selection acting on early size traits. Maternal genetic effects were significant at ages 0 and 1, having important evolutionary implications for early weight, but declined with age being negligible by age 2. Strong positive genetic correlations between age-specific traits suggest that selection on June weight at any age will likely induce positively correlated responses across ontogeny. Random regression modeling yielded similar results to traditional methods. However, by facilitating more efficient data use where phenotypic sampling is incomplete, random regression should allow better estimation of genetic (co)variances for size and growth traits in natural populations.     

Genetic architecture of survival and fitness-related traits in two populations of Atlantic salmon

The additive genetic effects of traits can be used to predict evolutionary trajectories, such as responses to selection. Non-additive genetic and maternal environmental effects can also change evolutionary trajectories and influence phenotypes, but these effects have received less attention by researchers. We partitioned the phenotypic variance of survival and fitness-related traits into additive genetic, non-additive genetic and maternal environmental effects using a full-factorial breeding design within two allopatric populations of Atlantic salmon (Salmo salar). Maternal environmental effects were large at early life stages, but decreased during development, with non-additive genetic effects being most significant at later juvenile stages (alevin and fry). Non-additive genetic effects were also, on average, larger than additive genetic effects. The populations, generally, did not differ in the trait values or inferred genetic architecture of the traits. Any differences between the populations for trait values could be explained by maternal environmental effects. We discuss whether the similarities in architectures of these populations is the result of natural selection across a common juvenile environment.     

Selection and genetic (co)variance in bighorn sheep

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

Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird

The timing of annual life‐history events affects survival and reproduction of all organisms. A changing environment can perturb phenological adaptations and an important question is if populations can evolve fast enough to track the environmental changes. Yet, little is known about selection and evolutionary potential of traits determining the timing of crucial annual events. Migratory species, which travel between different climatic regions, are particularly affected by global environmental changes. To increase our understanding of evolutionary potential and selection of timing traits, we investigated the quantitative genetics of arrival date at the breeding ground using a multigenerational pedigree of a natural great reed warbler (Acrocephalus arundinaceus) population. We found significant heritability of 16.4% for arrival date and directional selection for earlier arrival in both sexes acting through reproductive success, but not through lifespan. Mean arrival date advanced with 6 days over 20 years, which is in exact accordance with our predicted evolutionary response based on the breeder's equation. However, this phenotypic change is unlikely to be caused by microevolution, because selection seems mainly to act on the nongenetic component of the trait. Furthermore, demographical changes could also not account for the advancing arrival date. Instead, a strong correlation between spring temperatures and population mean arrival date suggests that phenotypic plasticity best explains the advancement of arrival date in our study population. Our study dissects the evolutionary and environmental forces that shape timing traits and thereby increases knowledge of how populations cope with rapidly changing environments.     

The effects of stress and sex on selection,genetic covariance,and the evolutionary response

The capacity of a population to adapt to selection (evolvability) depends on whether the structure of genetic variation permits the evolution of fitter trait combinations. Selection, genetic variance and genetic covariance can change under environmental stress, and males and females are not genetically independent, yet the combined effects of stress and dioecy on evolvability are not well understood. Here, we estimate selection, genetic (co)variance and evolvability in both sexes of Tribolium castaneum flour beetles under stressful and benign conditions, using a half‐sib breeding design. Although stress uncovered substantial latent heritability, stress also affected genetic covariance, such that evolvability remained low under stress. Sexual selection on males and natural selection on females favoured a similar phenotype, and there was positive intersex genetic covariance. Consequently, sexual selection on males augmented adaptation in females, and intralocus sexual conflict was weak or absent. This study highlights that increased heritability does not necessarily increase evolvability, suggests that selection can deplete genetic variance for multivariate trait combinations with strong effects on fitness, and tests the recent hypothesis that sexual conflict is weaker in stressful or novel environments.     

Dominance Genetic Variance for Traits Under Directional Selection in Drosophila serrata

In contrast to our growing understanding of patterns of additive genetic variance in single- and multi-trait combinations, the relative contribution of nonadditive genetic variance, particularly dominance variance, to multivariate phenotypes is largely unknown. While mechanisms for the evolution of dominance genetic variance have been, and to some degree remain, subject to debate, the pervasiveness of dominance is widely recognized and may play a key role in several evolutionary processes. Theoretical and empirical evidence suggests that the contribution of dominance variance to phenotypic variance may increase with the correlation between a trait and fitness; however, direct tests of this hypothesis are few. Using a multigenerational breeding design in an unmanipulated population of Drosophila serrata, we estimated additive and dominance genetic covariance matrices for multivariate wing-shape phenotypes, together with a comprehensive measure of fitness, to determine whether there is an association between directional selection and dominance variance. Fitness, a trait unequivocally under directional selection, had no detectable additive genetic variance, but significant dominance genetic variance contributing 32% of the phenotypic variance. For single and multivariate morphological traits, however, no relationship was observed between trait–fitness correlations and dominance variance. A similar proportion of additive and dominance variance was found to contribute to phenotypic variance for single traits, and double the amount of additive compared to dominance variance was found for the multivariate trait combination under directional selection. These data suggest that for many fitness components a positive association between directional selection and dominance genetic variance may not be expected.     

ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS

Life-history traits such as longevity and fecundity often show low heritability. This is usually interpreted in terms of Fisher's fundamental theorem to mean that populations are near evolutionary equilibrium and genetic variance in total fitness is low. We develop the causal relationship between metric traits and life-history traits to show that a life-history trait is expected to have a low heritability whether or not the population is at equilibrium. This is because it is subject to all the environmental variation in the metric traits that affect it plus additional environmental variation. There is no simple prediction regarding levels of additive genetic variance in life-history traits, which may be high at equilibrium. Several other patterns in the inheritance of life-history traits are readily predicted from the causal model. These include the strength of genetic correlations between life-history traits, levels of nonadditive genetic variance, and the inevitability of genotype-environment interaction.     

Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components

Despite great interest in sexual selection, relatively little is known in detail about the genetic and environmental determinants of secondary sexual characters in natural populations. Such information is important for determining the way in which populations may respond to sexual selection. We report analyses of genetic and large-scale environmental components of phenotypic variation of two secondary sexual plumage characters (forehead and wing patch size) in the collared flycatcher Ficedula albicollis over a 22-year period. We found significant heritability for both characters but little genetic covariance between the two. We found a positive association between forehead patch size and a large-scale climatic index, the North Atlantic Oscillation (NAO) index, but not for wing patch. This pattern was observed in both cross-sectional and longitudinal data suggesting that the population response to NAO index can be explained as the result of phenotypic plasticity. Heritability of forehead patch size for old males, calculated under favorable conditions (NAO index > or = median), was greater than that under unfavorable conditions (NAO index < median). These changes occurred because there were opposing changes in additive genetic variance (VA) and residual variance (VR) under favorable and unfavorable conditions, with VA increasing and VR decreasing in good environments. However, no such effect was detected for young birds, or for wing patch size in either age class. In addition to these environmental effects on both phenotypic and genetic variances, we found evidence for a significant decrease of forehead patch size over time in older birds. This change appears to be caused by a change in the sign of viability selection on forehead patch size, which is associated with a decline in the breeding value of multiple breeders. Our data thus reveal complex patterns of environmental influence on the expression of secondary sexual characters, which may have important implications for understanding selection and evolution of these characters.     

Stabilizing Selection for Pupa Weight in TRIBOLIUM CASTANEUM

Ninety-five generations of stabilizing selection for pupa weight in Tribolium castaneum resulted in a significant decrease in phenotypic variance, moderate reductions in additive genetic variance, but only slight changes in heritability for the trait. Sterility was significantly lower and the average number of live progeny per fertile mating was significantly higher in populations where stabilizing selection was practiced as compared with random selected populations. The results indicate that more genetic variability is being maintained than would be expected unless a fraction of the genes have a heterozygote advantage on the fitness scale. The reduction in phenotypic variance indicated that the populations with stablizing selection became somewhat more buffered against environmental sources of variation over the course of the experiment.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.