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.     

A general definition of the heritable variation that determines the potential of a population to respond to selection

Genetic selection is a major force shaping life on earth. In classical genetic theory, response to selection is the product of the strength of selection and the additive genetic variance in a trait. The additive genetic variance reflects a population's intrinsic potential to respond to selection. The ordinary additive genetic variance, however, ignores the social organization of life. With social interactions among individuals, individual trait values may depend on genes in others, a phenomenon known as indirect genetic effects. Models accounting for indirect genetic effects, however, lack a general definition of heritable variation. Here I propose a general definition of the heritable variation that determines the potential of a population to respond to selection. This generalizes the concept of heritable variance to any inheritance model and level of organization. The result shows that heritable variance determining potential response to selection is the variance among individuals in the heritable quantity that determines the population mean trait value, rather than the usual additive genetic component of phenotypic variance. It follows, therefore, that heritable variance may exceed phenotypic variance among individuals, which is impossible in classical theory. This work also provides a measure of the utilization of heritable variation for response to selection and integrates two well-known models of maternal genetic effects. The result shows that relatedness between the focal individual and the individuals affecting its fitness is a key determinant of the utilization of heritable variance for response to selection.     

Evolution of adaptive phenotypic variation patterns by direct selection for evolvability

A basic assumption of the Darwinian theory of evolution is that heritable variation arises randomly. In this context, randomness means that mutations arise irrespective of the current adaptive needs imposed by the environment. It is broadly accepted, however, that phenotypic variation is not uniformly distributed among phenotypic traits, some traits tend to covary, while others vary independently, and again others barely vary at all. Furthermore, it is well established that patterns of trait variation differ among species. Specifically, traits that serve different functions tend to be less correlated, as for instance forelimbs and hind limbs in bats and humans, compared with the limbs of quadrupedal mammals. Recently, a novel class of genetic elements has been identified in mouse gene-mapping studies that modify correlations among quantitative traits. These loci are called relationship loci, or relationship Quantitative Trait Loci (rQTL), and affect trait correlations by changing the expression of the existing genetic variation through gene interaction. Here, we present a population genetic model of how natural selection acts on rQTL. Contrary to the usual neo-Darwinian theory, in this model, new heritable phenotypic variation is produced along the selected dimension in response to directional selection. The results predict that selection on rQTL leads to higher correlations among traits that are simultaneously under directional selection. On the other hand, traits that are not simultaneously under directional selection are predicted to evolve lower correlations. These results and the previously demonstrated existence of rQTL variation, show a mechanism by which natural selection can directly enhance the evolvability of complex organisms along lines of adaptive change.     

A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker-based approaches have received attention because they can potentially be applied directly to wild populations. For long-lived, self-compatible plant species where pedigrees are inadequate, the regression-based method proposed by Ritland has the appeal of estimating heritabilities from marker-based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra-population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.     

Genetic isolation of fragmented populations is exacerbated by drift and selection

Reduced genetic variation at marker loci in small populations has been well documented, whereas the relationship between quantitative genetic variation and population size has attracted little empirical investigation. Here we demonstrate that both neutral and quantitative genetic variation are reduced in small populations of a fragmented plant metapopulation, and that both drift and selective change are enhanced in small populations. Measures of neutral genetic differentiation (F(ST)) and quantitative genetic differentiation (Q(ST)) in two traits were higher among small demes, and Q(ST) between small populations exceeded that expected from drift alone. This suggests that fragmented populations experience both enhanced genetic drift and divergent selection on phenotypic traits, and that drift affects variation in both neutral markers and quantitative traits. These results highlight the need to integrate natural selection into conservation genetic theory, and suggests that small populations may represent reservoirs of genetic variation adaptive within a wide range of environments.     

Patterns of natural selection on morphology of male and female collared flycatchers (Ficedula albicollis)

Natural selection may act in different directions among years, life stages, or classes of individuals. Fluctuating selection of this kind is potentially an important mechanism by which additive genetic variation for quantitative traits is maintained, and can prevent populations reaching local adaptive peaks. We analysed natural selection acting on three morphological traits of male and female collared flycatchers via both fecundity and survival, using 15 years' data from a large isolated population on Godand, Sweden. We particularly investigated variation in the direction and magnitude of selection acting: (1) among years over the study period; (2) on different life stages and (3) the consistency of observed patterns of selection with sexual size dimorphism (SSD) in this population. We found little evidence of natural selection on these traits over the study period. Evidence for directional, stabilizing and disruptive selection was found for some year-trait combinations, but these patterns were inconsistent with respect to both the magnitude and form of selection found. Consequently, our results, based on the detailed analysis of natural selection in a large wild population over a period of 15 years, provide evidence for the common assumption that forces of selection acting on quantitative traits are generally weak. They are also consistent with the suggestion that environmental stability is an important determinant of the degree to which organisms fit their environment.     

Genetic variability under mutation selection balance

A fundamental problem in evolutionary genetics is understanding how high levels of genetic variation in quantitative traits are maintained in natural populations. Variation is removed by the natural selection of individuals with optimal phenotypes and is recovered by mutation; however, previous analyses had indicated that a mutation-selection balance was insufficient to maintain observed levels of genetic variation in these traits. Using more general models, however, it has recently been shown that it is indeed a sufficient mechanism. These models can be used to explore other phenomena in evolutionary biology.     

The quantitative genetics of the prevalence of infectious diseases: hidden genetic variation due to indirect genetic effects dominates heritable variation and response to selection

Infectious diseases have profound effects on life, both in nature and agriculture. However, a quantitative genetic theory of the host population for the endemic prevalence of infectious diseases is almost entirely lacking. While several studies have demonstrated the relevance of transmission of infections for heritable variation and response to selection, current quantitative genetics ignores transmission. Thus, we lack concepts of breeding value and heritable variation for endemic prevalence, and poorly understand response of endemic prevalence to selection. Here, we integrate quantitative genetics and epidemiology, and propose a quantitative genetic theory for the basic reproduction number R₀ and for the endemic prevalence of an infection. We first identify the genetic factors that determine the prevalence. Subsequently, we investigate the population-level consequences of individual genetic variation, for both R0 and the endemic prevalence. Next, we present expressions for the breeding value and heritable variation, for endemic prevalence and individual binary disease status, and show that these depend strongly on the prevalence. Results show that heritable variation for endemic prevalence is substantially greater than currently believed, and increases strongly when prevalence decreases, while heritability of disease status approaches zero. As a consequence, response of the endemic prevalence to selection for lower disease status accelerates considerably when prevalence decreases, in contrast to classical predictions. Finally, we show that most heritable variation for the endemic prevalence is hidden in indirect genetic effects, suggesting a key role for kin-group selection in the evolutionary history of current populations and for genetic improvement in animals and plants.     

Relaxation of herbivore‐mediated selection drives the evolution of genetic covariances between plant competitive and defense traits

Insect herbivores are important mediators of selection on traits that impact plant defense against herbivory and competitive ability. Although recent experiments demonstrate a central role for herbivory in driving rapid evolution of defense and competition‐mediating traits, whether and how herbivory shapes heritable variation in these traits remains poorly understood. Here, we evaluate the structure and evolutionary stability of the G matrix for plant metabolites that are involved in defense and allelopathy in the tall goldenrod, Solidago altissima. We show that G has evolutionarily diverged between experimentally replicated populations that evolved in the presence versus the absence of ambient herbivory, providing direct evidence for the evolution of G by natural selection. Specifically, evolution in an herbivore‐free habitat altered the orientation of G , revealing a negative genetic covariation between defense‐ and competition‐related metabolites that is typically masked in herbivore‐exposed populations. Our results may be explained by predictions of classical quantitative genetic theory, as well as the theory of acquisition‐allocation trade‐offs. The study provides compelling evidence that herbivory drives the evolution of plant genetic architecture.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

Heritability,covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment

This study explored genetic variation and co‐variation in multiple functional plant traits. Our goal was to characterize selection, heritabilities and genetic correlations among different types of traits to gain insight into the evolutionary ecology of plant populations and their interactions with insect herbivores. In a field experiment, we detected significant heritable variation for each of 24 traits of Oenothera biennis and extensive genetic covariance among traits. Traits with diverse functions formed several distinct groups that exhibited positive genetic covariation with each other. Genetic variation in life‐history traits and secondary chemistry together explained a large proportion of variation in herbivory (r² = 0.73). At the same time, selection acted on lifetime biomass, life‐history traits and two secondary compounds of O. biennis, explaining over 95% of the variation in relative fitness among genotypes. The combination of genetic covariances and directional selection acting on multiple traits suggests that adaptive evolution of particular traits is constrained, and that correlated evolution of groups of traits will occur, which is expected to drive the evolution of increased herbivore susceptibility. As a whole, our study indicates that an examination of genetic variation and covariation among many different types of traits can provide greater insight into the evolutionary ecology of plant populations and plant–herbivore interactions.     

A general model of the relation between phenotypic selection and genetic response

The phenotypic view of selection assumes that genetic responses can be predicted from selective forces and heritability — or in the classical quantitative genetic equation: R = h²S. However, data on selection in bird populations show that often no selection responses is found, despite consistent selective forces on phenotypes and significant heritable variation. Such discrepancies may arise due to the assumption that selection only acts on observed phenotypes. We derive a general selection equation that takes into account the possibility that some relevant (internal or external) traits are not measured. This equation shows that the classic equation applies if selection directly acts on the measured, phenotypic traits. This is not the case when, for instance, there are unknown internal genetic trade-offs, or unknown common environmental factors affecting both trait and fitness. In such cases, any relationship between phenotypic selection and genetic response is possible. Fortunately, the classical model can be tested by comparing phenotypic and genetic covariances between traits and fitness; an indication that important internal or external traits are missing can thus be obtained. Such an analysis was indeed found in the literature; for selection on fledging weight in Great Tits it yielded valuable extra information.     

Characterizing the evolution of genetic variance using genetic covariance tensors

Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance–covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.     

Natural selection and quantitative genetics of life-history traits in Western women: a twin study

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection will cause a change among women in a contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the "baby boom" phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.     

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.     

Artificial selection reveals heritable variation for developmental instability

Fluctuating (nondirectional) asymmetry (FA) of bilaterally paired structures on a symmetrical organism is commonly used to assay the developmental instability (DI) caused by environmental or genetic factors. Although evidence for natural selection to reduce FA has been reported, evidence that FA (and by extension DI) is heritable is weak. We report the use of artificial selection to demonstrate heritable variation in the fluctuating asymmetry of interlandmark distances within the wing in an outbred population of Drosophila melanogaster. Our estimates for the heritability of FA range from 0% to 1% and result in estimates for the heritability of DI as large as 20%, comparable to values typical for life-history traits. These values indicate the existence of evolutionarily relevant genetic variation for DI and the effectiveness of selection for reduced FA suggests that natural selection has not fixed all the genetic variants that would improve developmental stability in these populations.     

Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data

The relative roles of natural selection and direct environmental induction, as well as of natural selection and genetic drift, in creating clinal latitudinal variation in quantitative traits have seldom been assessed in vertebrates. To address these issues, we compared molecular and quantitative genetic differentiation between six common frog (Rana temporaria) populations along an approximately 1600 km long latitudinal gradient across Scandinavia. The degree of population differentiation (QST approximately 0.81) in three heritable quantitative traits (age and size at metamorphosis, growth rate) exceeded that in eight (neutral) microsatellite loci (FST = 0.24). Isolation by distance was clear for both neutral markers and quantitative traits, but considerably stronger for one of the three quantitative traits than for neutral markers. QST estimates obtained using animals subjected to different rearing conditions (temperature and food treatments) revealed some environmental dependency in patterns of population divergence in quantitative traits, but in general, these effects were weak in comparison to overall patterns. Pairwise comparisons of FST and QST estimates across populations and treatments revealed that the degree of quantitative trait differentiation was not generally predictable from knowledge of that in molecular markers. In fact, both positive and negative correlations were observed depending on conditions where the quantitative genetic variability had been measured. All in all, the results suggest a very high degree of genetic subdivision both in neutral marker genes and genes coding quantitative traits across a relatively recently (< 9000 years) colonized environmental gradient. In particular, they give evidence for natural selection being the primary agent behind the observed latitudinal differentiation in quantitative traits.     

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.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.