Xu-Sheng Zhang

EVOLUTION OF THE ENVIRONMENTAL COMPONENT OF THE PHENOTYPIC VARIANCE: STABILIZING SELECTION IN CHANGING ENVIRONMENTS AND THE COST OF HOMOGENEITY

Abstract Quantitative traits show abundant genetic, environmental, and phenotypic variance, yet if they are subject to stabilizing selection for an optimal phenotype, both the genetic and environmental components are expected to decline. The mechanisms that determine the level and maintenance of phenotypic variance are not yet fully understood. While there has been extensive study of mechanisms maintaining genetic variability, it has generally been assumed that environmental variance is not dependent on the genotype and therefore not subject to change. However, accumulating data suggest that the environmental variance is under some degree of genetic control. In this study, it is assumed accordingly that both the genotypic value (i.e., mean phenotypic value) and the variance of phenotypic value given genotypic value depend on the genotype. Two models are investigated as potentially able to explain the protected maintenance of environmental variance of quantitative traits under stabilizing selection. One is varying environment among generations such that both the optimal phenotype and the strength of the stabilizing selection vary between generations. The other is the cost of homogeneity, which is based on an assumption of an engineering cost of minimizing variability in development. It is shown that a small homogeneity cost is enough to maintain the observed levels of environmental variance, whereas a large amount of temporal variation in the optimal phenotype and the strength of selection would be necessary.

Effects on phenotypic variability of directional selection arising through genetic differences in residual variability

In standard models of quantitative traits, genotypes are assumed to differ in mean but not variance of the trait. Here we consider directional selection for a quantitative trait for which genotypes also confer differences in variability, viewed either as differences in residual phenotypic variance when individual loci are concerned or as differences in environmental variability when the whole genome is considered. At an individual locus with additive effects, the selective value of the increasing allele is given by ia/sigma + 1/2 ixb/sigma2, where i is the selection intensity, x is the standardized truncation point, sigma2 is the phenotypic variance, and a/sigma and b/sigma2 are the standardized differences in mean and variance respectively between genotypes at the locus. Assuming additive effects on mean and variance across loci, the response to selection on phenotype in mean is isigma2(Am)/sigma + 1/2 ixcov(Amv)/sigma2 and in variance is icov(Amv)/sigma + 1/2 ixsigma2(Av)/sigma2, where sigma2(Am) is the (usual) additive genetic variance of effects of genes on the mean, sigma2(Av) is the corresponding additive genetic variance of their effects on the variance, and cov(Amv) is the additive genetic covariance of their effects. Changes in variance also have to be corrected for any changes due to gene frequency change and for the Bulmer effect, and relevant formulae are given. It is shown that effects on variance are likely to be greatest when selection is intense and when selection is on individual phenotype or within family deviation rather than on family mean performance. The evidence for and implications of such variability in variance are discussed.

On the Pleiotropic Structure of the Genotype–phenotype Map and the Evolvability of Complex Organisms

Analyses of effects of mutants on many traits have enabled estimates to be obtained of the magnitude of pleiotropy, and in reviews of such data others have concluded that the degree of pleiotropy is highly restricted, with implications on the evolvability of complex organisms. We show that these conclusions are highly dependent on statistical assumptions, for example significance levels. We analyze models with pleiotropic effects on all traits at all loci but by variable amounts, considering distributions of numbers of traits declared significant, overall pleiotropic effects, and extent of apparent modularity of effects. We demonstrate that these highly pleiotropic models can give results similar to those obtained in analyses of experimental data and that conclusions on limits to evolvability through pleiotropy are not robust.

Influence of Dominance, Leptokurtosis and Pleiotropy of Deleterious Mutations on Quantitative Genetic Variation at Mutation-Selection Balance

In models of maintenance of genetic variance (VG) it has often been assumed that mutant alleles act additively. However, experimental data show that the dominance coefficient varies among mutant alleles and those of large effect tend to be recessive. On the basis of empirical knowledge of mutations, a joint-effect model of pleiotropic and real stabilizing selection that includes dominance is constructed and analyzed. It is shown that dominance can dramatically alter the prediction of equilibrium VG. Analysis indicates that for the situations where mutations are more recessive for fitness than for a quantitative trait, as supported by the available data, the joint-effect model predicts a significantly higher VG than does an additive model. Importantly, for what seem to be realistic distributions of mutational effects (i.e., many mutants may not affect the quantitative trait substantially but are likely to affect fitness), the observed high levels of genetic variation in the quantitative trait under strong apparent stabilizing selection can be generated. This investigation supports the hypothesis that most VG comes from the alleles nearly neutral for fitness in heterozygotes while apparent stabilizing selection is contributed mainly by the alleles of large effect on the quantitative trait. Thus considerations of dominance coefficients of mutations lend further support to our previous conclusion that mutation-selection balance is a plausible mechanism of the maintenance of the genetic variance in natural populations.

MULTIVARIATE STABILIZING SELECTION AND PLEIOTROPY IN THE MAINTENANCE OF QUANTITATIVE GENETIC VARIATION

Abstract. We investigate maintenance of quantitative genetic variation at mutation‐selection balance for multiple traits. The intrinsic strength of real stabilizing selection on one of these traits denoted the “target trait” and the observed strength of apparent stabilizing selection on the target trait can be quite different: the latter, which is estimable, is much smaller (i.e., implying stronger selection) than the former. Distinguishing them may enable the mutation load to be relaxed when considering multivariate stabilizing selection. It is shown that both correlations among mutational effects and among strengths of real stabilizing selection on the traits are not important unless they are high. The analysis for independent situations thus provides a good approximation to the case where mutant and stabilizing selection effects are correlated. Multivariate stabilizing selection can be regarded as a combination of stabilizing selection on the target trait and the pleiotropic direct selection on fitness that is solely due to the effects of real stabilizing selection on the hidden traits. As the overall fitness approaches a constant value as the number of traits increases, multivariate stabilizing selection can maintain abundant genetic variance only under quite weak selection. The common observations of high polygenic variance and strong stabilizing selection thus imply that if the mutation‐selection balance is the true mechanism of maintenance of genetic variation, the apparent stabilizing selection cannot arise solely by real stabilizing selection simultaneously on many metric traits.

Mutation‐Selection Balance for Environmental Variance

The role of mutation‐selection balance in maintaining environmental variance (VE) of quantitative traits is investigated under the assumption that genotypes differ in the magnitude of phenotypic variance, given genotypic value. Thus, VE can be regarded as a quantitative trait. As stabilizing selection on phenotype favors genotypes contributing low VE, mutations that decrease VE are more likely to become fixed than those that increase it, and therefore VE should decline. If, however, essentially all mutants increase VE and overall selection is sufficiently strong that no mutants become fixed, then VE can be maintained. The heritability of the trait is determined by the relative sizes of mutational effects on phenotypic mean and residual variance and is independent of mutation rate and pleiotropic effects. This conclusion is not robust for small populations because some mutants may become fixed, which indicates that other selective forces must be involved, such as an intrinsic cost of homogeneity.

THE PHENOTYPIC VARIANCE WITHIN PLASTIC TRAITS UNDER MIGRATION-MUTATION-SELECTION BALANCE

Abstract How phenotypic variances of quantitative traits are influenced by the heterogeneity in environment is an important problem in evolutionary biology. In this study, both genetic and environmental variances in a plastic trait under migration‐mutation‐stabilizing selection are investigated. For this, a linear reaction norm is used to approximate the mapping from genotype to phenotype, and a population of clonal inheritance is assumed to live in a habitat consisting of many patches in which environmental conditions vary among patches and generations. The life cycle is assumed to be selection‐reproduction‐mutation‐migration. Analysis shows that phenotypic plasticity is adaptive if correlations between the optimal phenotype and environment have become established in both space and/or time, and it is thus possible to maintain environmental variance (VE) in the plastic trait. Under the special situation of no mutation but maximum migration such that separate patches form an effective single‐site habitat, the genotype that maximizes the geometric mean fitness will come to fixation and thus genetic variance (VG) cannot be maintained. With mutation and/or restricted migration, VG can be maintained and it increases with mutation rate but decreases with migration rate; whereas VE is little affected by them. Temporal variation in environmental quality increases VG while its spatial variance decreases VG. Variation in environmental conditions may decrease the environmental variance in the plastic trait.

FISHER'S GEOMETRICAL MODEL OF FITNESS LANDSCAPE AND VARIANCE IN FITNESS WITHIN A CHANGING ENVIRONMENT

The fitness of an individual can be simply defined as the number of its offspring in the next generation. However, it is not well understood how selection on the phenotype determines fitness. In accordance with Fishers fundamental theorem, fitness should have no or very little genetic variance, whereas empirical data suggest that is not the case. To bridge these knowledge gaps, we follow Fishers geometrical model and assume that fitness is determined by multivariate stabilizing selection toward an optimum that may vary among generations. We assume random mating, free recombination, additive genes, and uncorrelated stabilizing selection and mutational effects on traits. In a constant environment, we find that genetic variance in fitness under mutation‐selection balance is a U‐shaped function of the number of traits (i.e., of the so‐called “organismal complexity”). Because the variance can be high if the organism is of either low or high complexity, this suggests that complexity has little direct costs. Under a temporally varying optimum, genetic variance increases relative to a constant optimum and increasingly so when the mutation rate is small. Therefore, mutation and changing environment together can maintain high genetic variance. These results therefore lend support to Fishers geometric model of a fitness landscape.

COMPETITION CAN MAINTAIN GENETIC BUT NOT ENVIRONMENTAL VARIANCE IN THE PRESENCE OF STABILIZING SELECTION

Abstract A population in which there is stabilizing selection acting on quantitative traits toward an intermediate optimum becomes monomorphic in the absence of mutation. Further, genotypes that show least environmental variation are also favored, such that selection is likely to reduce both genetic and environmental components of phenotypic variance. In contrast, intraspecific competition for resources is more severe between phenotypically similar individuals, such that those deviating from prevailing phenotypes have a selective advantage. It has been shown previously that polymorphism and phenotypic variance can be maintained if competition between individuals is “effectively” stronger than stabilizing selection. Environmental variance is generally observed in quantitative traits, so mechanisms to explain its maintenance are sought, but the impact of competition on its magnitude has not previously been studied. Here we assume that a quantitative trait is subject to selection for an optimal value and to selection due to competition. Further, we assume that both the mean and variance of the phenotypic value depend on genotype, such that both may be affected by selection. Theoretical analysis and numerical simulations reveal that environmental variance can be maintained only when the genetic variance (in mean phenotypic value) is constrained to a very low level. Environmental variance will be replaced entirely by genotypic variance if a range of genotypes that vary widely in mean phenotype are present or become so by mutation. The distribution of mean phenotypic values is discrete when competition is strong relative to stabilizing selection; but more genotypes segregate and the distribution can approach continuity as competition becomes extremely strong. If the magnitude of the environmental variance is not under genetic control, there is a complementary relationship between the levels of environmental and genetic variance such that the level of phenotypic variance is little affected.

Change and maintenance of variation in quantitative traits in the context of the Price equation

The Price equation is a general description of evolutionary change in any character from one generation to the next due to natural selection and other forces such as mutation and recombination. Recently it has been widely utilised in many fields including quantitative genetics, but these applications have focused mainly on the response to selection in the mean of characters. Many different and, in some cases, conflicting models have been investigated by quantitative geneticists to examine the change and maintenance of both genetic and environmental variance of quantitative traits under selection and other forces. In this study, we use the Price equation to derive many such well-known results for the dynamics and equilibria of variances in a straightforward way and to develop them further.