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.     

Apparent directional selection by biased pleiotropic mutation

Pleiotropic effects of deleterious mutations are considered to be among the factors responsible for genetic constraints on evolution by long-term directional selection acting on a quantitative trait. If pleiotropic phenotypic effects are biased in a particular direction, mutations generate apparent directional selection, which refers to the covariance between fitness and the trait owing to a linear association between the number of mutations possessed by individuals and the genotypic values of the trait. The present analysis has shown how the equilibrium mean value of the trait is determined by a balance between directional selection and biased pleiotropic mutations. Assuming that genes act additively both on the trait and on fitness, the total variance-standardized directional selection gradient was decomposed into apparent and true components. Experimental data on mutation bias from the bristle traits of Drosophila and life history traits of Daphnia suggest that apparent selection explains a small but significant fraction of directional selection pressure that is observed in nature; the data suggest that changes induced in a trait by biased pleiotropic mutation (i.e., by apparent directional selection) are easily compensated for by (true) directional selection.     

Tests of adaptation: functional studies of pollen removal and estimates of natural selection on anther position in wild radish

Background

There are a number of difficulties associated with the study of adaptation. One is a lack of variation in the trait, which is common in adaptations because past selection has removed unfit variants. This lack of variation makes it difficult to determine the relationship between trait variation and fitness. Another difficulty is proving causation in this trait–fitness relationship, because a correlated trait might be the actual adaptation. These difficulties can be ameliorated at least partially by combining studies of natural variation with studies of experimentally manipulated traits and traits whose variance has been augmented by artificial selection.

Scope

We review here a number of our studies on the adaptive value of two aspects of anther position in wild radish (Raphanus raphanistrum, Brassicaceae): anther exsertion, i.e. the degree to which anthers protrude from the mouth of the corolla tube, and anther height dimorphism, i.e. the difference in lengths of the filaments between the two short and four long stamens. We have used both functional analyses, in which the response variable is pollen removal, and measurements of selection, in which the response variable is lifetime male fitness estimated by molecular genetic paternity analyses. In these studies we use both the natural variation in populations as well as manipulated variation, the latter through both stamen removal and artificial selection, to re-create the ancestral trait conditions.

Conclusions

Our work provides convincing evidence that intermediate anther exsertion values are adaptive, and that this is probably an adaptation to a subset of the pollinator fauna, small bees. The picture for anther height dimorphism is much less clear, as the weight of current evidence suggests that current values of this trait might actually be maladaptive; however, if this is true it is difficult to understand how the dimorphism is maintained across the family Brassicaceae.Key words: Wild radish, Raphanus raphanistrum, adaptation, natural selection, anther position, pollination, pollen removal     

REDUCED GENETIC VARIANCE AMONG HIGH FITNESS INDIVIDUALS: INFERRING STABILIZING SELECTION ON MALE SEXUAL DISPLAYS IN DROSOPHILA SERRATA

Directional selection is prevalent in nature, yet phenotypes tend to remain relatively constant, suggesting a limit to trait evolution. However, the genetic basis of this limit is unresolved. Given widespread pleiotropy, opposing selection on a trait may arise from the effects of the underlying alleles on other traits under selection, generating net stabilizing selection on trait genetic variance. These pleiotropic costs of trait exaggeration may arise through any number of other traits, making them hard to detect in phenotypic analyses. Stabilizing selection can be inferred, however, if genetic variance is greater among low‐ compared to high‐fitness individuals. We extend a recently suggested approach to provide a direct test of a difference in genetic variance for a suite of cuticular hydrocarbons (CHCs) in Drosophila serrata. Despite strong directional sexual selection on these traits, genetic variance differed between high‐ and low‐fitness individuals and was greater among the low‐fitness males for seven of eight CHCs, significantly more than expected by chance. Univariate tests of a difference in genetic variance were nonsignificant but likely have low power. Our results suggest that further CHC exaggeration in D. serrata in response to sexual selection is limited by pleiotropic costs mediated through other traits.     

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.     

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.     

Very low levels of direct additive genetic variance in fitness and fitness components in a red squirrel population

A trait must genetically correlate with fitness in order to evolve in response to natural selection, but theory suggests that strong directional selection should erode additive genetic variance in fitness and limit future evolutionary potential. Balancing selection has been proposed as a mechanism that could maintain genetic variance if fitness components trade off with one another and has been invoked to account for empirical observations of higher levels of additive genetic variance in fitness components than would be expected from mutation–selection balance. Here, we used a long‐term study of an individually marked population of North American red squirrels (Tamiasciurus hudsonicus) to look for evidence of (1) additive genetic variance in lifetime reproductive success and (2) fitness trade‐offs between fitness components, such as male and female fitness or fitness in high‐ and low‐resource environments. “Animal model” analyses of a multigenerational pedigree revealed modest maternal effects on fitness, but very low levels of additive genetic variance in lifetime reproductive success overall as well as fitness measures within each sex and environment. It therefore appears that there are very low levels of direct genetic variance in fitness and fitness components in red squirrels to facilitate contemporary adaptation in this population.     

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.     

An experimental assessment of artificial within-family selection for fitness in conservation programs

Equalizing familiar contributions is the simplest recommended strategy to maintain genetic diversity in conservation programs. However, this method implies a relaxation of natural selection and the possibility of accumulation of deleterious mutations. Computer simulations have shown that performing selection within families for fitness traits in a conservation program can be useful to alleviate such problems. We thus carried out an experiment with the model species Drosophila melanogaster in order to assess whether or not selection for fitness traits can be useful. We considered a fitness trait (pupa productivity) that was first checked to perform as a typical fitness component. The trait showed an inbreeding depression of 1.2 per 1 % increase in inbreeding and an asymmetrical response to selection with average realized heritabilities of about 0.04 in the upward direction and an order of magnitude larger (0.36) in the downward direction. The management experiment indicated that artificial within-family selection for fitness had only a marginal success for two reasons. First, there was not an appreciable decline in fitness across the experiment despite the low population sizes assumed (N = 10 or 20), even in the population not subjected to selection. This result is compatible with fitness models which imply the segregation of few deleterious mutations of large effect. Second, artificial selection within families had a limited impact on the trait, as one expects for a typical fitness component with very low heritability.     

Improvement of Rice Biomass Yield through QTL-Based Selection

Biomass yield of rice (Oryza sativa L.) is an important breeding target, yet it is not easy to improve because the trait is complex and phenotyping is laborious. Using progeny derived from a cross between two high-yielding Japanese cultivars, we evaluated whether quantitative trait locus (QTL)-based selection can improve biomass yield. As a measure of biomass yield, we used plant weight (aboveground parts only), which included grain weight and stem and leaf weight. We measured these and related traits in recombinant inbred lines. Phenotypic values for these traits showed a continuous distribution with transgressive segregation, suggesting that selection can affect plant weight in the progeny. Four significant QTLs were mapped for plant weight, three for grain weight, and five for stem and leaf weight (at α = 0.05); some of them overlapped. Multiple regression analysis showed that about 43% of the phenotypic variance of plant weight was significantly explained (P < 0.0001) by six of the QTLs. From F₂ plants derived from the same parental cross as the recombinant inbred lines, we divergently selected lines that carried alleles with positive or negative additive effects at these QTLs, and performed successive selfing. In the resulting F₆ lines and parents, plant weight significantly differed among the genotypes (at α = 0.05). These results demonstrate that QTL-based selection is effective in improving rice biomass yield.     

Expression of genetic and environmental variation during ageing

Summary A selection experiment with Drosophila melanogaster was carried out to test some theories of ageing by calculating genetic parameters for a reproductive fitness trait at different ages. Successful selection for increased lifespan showed that longevity is a trait under genetic control. Positive genetic correlations between early and late fitness were found. These results do not support the pleiotropy theory of ageing which predicts a negative genetic correlation. Both environmental and additive genetic variation clearly increased with age. Increased environmental variation probably reflects the individuals' difficulties in coping with environmental stress. The increase in additive genetic variation supports the mutation accumulation theory of ageing, as well as other theories that postulate increased additive genetic variation with age.     

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.     

Multiple regression for molecular-marker,quantitative trait data from large F2 populations

Molecular marker-quantitative trait associations are important for breeders to recognize and understand to allow application in selection. This work was done to provide simple, intuitive explanations of trait-marker regression for large samples from an F₂ and to examine the properties of the regression estimators. Beginning with a(- 1,0,1) coding of marker classes and expected frequencies in the F₂, expected values, variances, and covariances of marker variables were calculated. Simple linear regression and regression of trait values on two markers were computed. The sum of coefficient estimates for the flanking-marker regression is asymptotically unbiased for an included additive effect with complete interference, and is only slightly biased with no interference and moderately close (15 cM) marker spacing. The variance of the sum of regression coefficients is much more stable for small recombination distances than variances of individual coefficients. Multiple regression of trait variables on coded marker variables can be interpreted as the product of the inverse of the marker correlation matrix R and the vector a of simple linear regression estimators for each marker. For no interference, elements of the correlation matrix R can be written as products of correlations between adjacent markers. The inverse of R is displayed and used to illustrate the solution vector. Only markers immediately flanking trait loci are expected to have non-zero values and, with at least two marker loci between each trait locus, the solution vector is expected to be the sum of solutions for each trait locus. Results of this work should allow breeders to test for intervals in which trait loci are located and to better interpret results of the trait-marker regression.     

Mutation load and mutation-selection-balance in quantitative genetic traits

Haldane (1937) showed that the reduction of equilibrium mean fitness in an infinite population due to recurrent deleterious mutations depends only on the mutation rate but not on the harmfulness of mutants. His analysis, as well as more recent ones (cf. Crow 1970), ignored back mutation. The purpose of the present paper is to extend these results to arbitrary mutation patterns among alleles and to quantitative genetic traits. We derive first-order approximations for the equilibrium mean fitness (and the mutation load) and determine the order of the error term. For a metric trait under mutation-stabilizing-selection balance our result differs qualitatively from that of Crow and Kimura (1964), whose analysis is based on a Gaussian assumption. Our general approach also yields a mathematical proof that the variance under the usual mutation-stabilizing-selection model is, to first order, µ/s (the house-of-cards approximation) as µ/s tends to zero. This holds for arbitrary mutant distributions and does not require that the population mean coincide with the optimum. We show how the mutant distribution determines the order of the error term, and thus the accuracy of the house-of-cards approximation. Upper and lower bounds to the equilibrium variance are derived that deviate only to second order as µ/s tends to zero. The multilocus case is treated under the assumption of global linkage equilibrium.     

Multiple-Trait Genomic Selection Methods Increase Genetic Value Prediction Accuracy

Genetic correlations between quantitative traits measured in many breeding programs are pervasive. These correlations indicate that measurements of one trait carry information on other traits. Current single-trait (univariate) genomic selection does not take advantage of this information. Multivariate genomic selection on multiple traits could accomplish this but has been little explored and tested in practical breeding programs. In this study, three multivariate linear models (i.e., GBLUP, BayesA, and BayesCπ) were presented and compared to univariate models using simulated and real quantitative traits controlled by different genetic architectures. We also extended BayesA with fixed hyperparameters to a full hierarchical model that estimated hyperparameters and BayesCπ to impute missing phenotypes. We found that optimal marker-effect variance priors depended on the genetic architecture of the trait so that estimating them was beneficial. We showed that the prediction accuracy for a low-heritability trait could be significantly increased by multivariate genomic selection when a correlated high-heritability trait was available. Further, multiple-trait genomic selection had higher prediction accuracy than single-trait genomic selection when phenotypes are not available on all individuals and traits. Additional factors affecting the performance of multiple-trait genomic selection were explored.     

Pleiotropic Models of Polygenic Variation, Stabilizing Selection, and Epistasis

We show that in polymorphic populations many polygenic traits pleiotropically related to fitness are expected to be under apparent ``stabilizing selection' independently of the real selection acting on the population. This occurs, for example, if the genetic system is at a stable polymorphic equilibrium determined by selection and the nonadditive contributions of the loci to the trait value either are absent, or are random and independent of those to fitness. Stabilizing selection is also observed if the polygenic system is at an equilibrium determined by a balance between selection and mutation (or migration) when both additive and nonadditive contributions of the loci to the trait value are random and independent of those to fitness. We also compare different viability models that can maintain genetic variability at many loci with respect to their ability to account for the strong stabilizing selection on an additive trait. Let V(m) be the genetic variance supplied by mutation (or migration) each generation, V(g) be the genotypic variance maintained in the population, and n be the number of the loci influencing fitness. We demonstrate that in mutation (migration)-selection balance models the strength of apparent stabilizing selection is order V(m)/V(g). In the overdominant model and in the symmetric viability model the strength of apparent stabilizing selection is approximately 1/(2n) that of total selection on the whole phenotype. We show that a selection system that involves pairwise additive by additive epistasis in maintaining variability can lead to a lower genetic load and genetic variance in fitness (approximately 1/(2n) times) than an equivalent selection system that involves overdominance. We show that, in the epistatic model, the apparent stabilizing selection on an additive trait can be as strong as the total selection on the whole phenotype.     

Multilevel selection and the partitioning of covariance: a comparison of three approaches

Where the evolution of a trait is affected by selection at more than one hierarchical level, it is often useful to compare the magnitude of selection at each level by asking how much of the total evolutionary change is attributable to each level of selection. Three statistical partitioning techniques, each designed to answer this question, are compared, in relation to a simple multilevel selection model in which a trait's evolution is affected by both individual and group selection. None of the three techniques is wholly satisfactory: one implies that group selection can operate even if individual fitness is determined by individual phenotype alone, whereas the other two imply that group selection can operate even if there is no variance in group fitness. This has significant implications both for our understanding of what the term "multilevel selection" means and for the traditional concept of group selection.     

Quasi-independence, fitness, and advantageousness

I argue that the idea of ‘quasi-independence’ [Lewontin, R. C. (1978). Adaptation. Scientific American, 239(3), 212–230] cannot be understood without attending to the distinction between fitness and advantageousness [Sober, E. (1993). Philosophy of biology. Boulder: Westview Press]. Natural selection increases the frequency of fitter traits, not necessarily of advantageous ones. A positive correlation between an advantageous trait and a disadvantageous one may prevent the advantageous trait from evolving. The quasi-independence criterion is aimed at specifying the conditions under which advantageous traits will evolve by natural selection in this type of situation. Contrary to what others have argued [Sterelny, K. (1992). Evolutionary explanations of human behavior. Australian Journal of Philosophy, 70(2), 156–172, and Sterelny, K., &; Griffiths, P. (1999). Sex and death. Chicago: University of Chicago Press], these conditions must involve a precise quantitative measure of (a) the extent to which advantageous traits are beneficial, and (b) the degree to which they are correlated with other traits. Driscoll (2004) [Driscoll, C. (2004). Can behaviors be adaptations? Philosophy of Science, 71, 16–35] recognizes the need for such a measure, but I argue that she does not provide the correct formulation. The account of quasi-independence that I offer clarifies this point.     

Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at "Evolution Canyon", Mount Carmel, Israel

Background

Adaptation is an evolutionary process in which traits in a population are tailored by natural selection to better meet the challenges presented by the local environment. The major discussion relating to natural selection concerns the portraying of the cause and effect relationship between a presumably adaptive trait and selection agents generating it. Therefore, it is necessary to identify trait(s) that evolve in direct response to selection, enhancing the organism''s fitness. “Evolution Canyon” (EC) in Israel mirrors a microcosmic evolutionary system across life and is ideal to study natural selection and local adaptation under sharply, microclimatically divergent environments. The south-facing, tropical, sunny and xeric “African” slope (AS) receives 200%–800% higher solar radiation than the north-facing, temperate, shady and mesic “European” slope (ES), 200 meters apart. Thus, solar ultraviolet radiation (UVR) is a major selection agent in EC influencing the organism-environment interaction. Melanin is a trait postulated to have evolved for UV-screening in microorganisms. Here we investigate the cause and effect relationship between differential UVR on the opposing slopes of EC and the conidial melanin concentration of the filamentous soil fungus Aspergillus niger. We test the working hypothesis that the AS strains exhibit higher melanin content than strains from the ES resulting in higher UV resistance.

Methodology/Principal Findings

We measured conidial melanin concentration of 80 strains from the EC using a spectrophotometer. The results indicated that mean conidial melanin concentration of AS strains were threefold higher than ES strains and the former resisted UVA irradiation better than the latter. Comparisons of melanin in the conidia of A. niger strains from sunny and shady microniches on the predominantly sunny AS and predominantly shady ES indicated that shady conditions on the AS have no influence on the selection on melanin; in contrast, the sunny strains from the ES displayed higher melanin concentrations.

Conclusions/Significance

We conclude that melanin in A. niger is an adaptive trait against UVR generated by natural selection.     

Intraspecific trait variation influences physiological performance and fitness in the South Africa shrub genus Protea (Proteaceae)

Background and AimsGlobal plant trait datasets commonly identify trait relationships that are interpreted to reflect fundamental trade-offs associated with plant strategies, but often these trait relationships are not identified when evaluating them at smaller taxonomic and spatial scales. In this study we evaluate trait relationships measured on individual plants for five widespread Protea species in South Africa to determine whether broad-scale patterns of structural trait (e.g. leaf area) and physiological trait (e.g. photosynthetic rates) relationships can be detected within natural populations, and if these traits are themselves related to plant fitness.MethodsWe evaluated the variance structure (i.e. the proportional intraspecific trait variation relative to among-species variation) for nine structural traits and six physiological traits measured in wild populations. We used a multivariate path model to evaluate the relationships between structural traits and physiological traits, and the relationship between these traits and plant size and reproductive effort.Key ResultsWhile intraspecific trait variation is relatively low for structural traits, it accounts for between 50 and 100 % of the variation in physiological traits. Furthermore, we identified few trait associations between any one structural trait and physiological trait, but multivariate regressions revealed clear associations between combinations of structural traits and physiological performance (R² = 0.37–0.64), and almost all traits had detectable associations with plant fitness.ConclusionsIntraspecific variation in structural traits leads to predictable differences in individual-level physiological performance in a multivariate framework, even though the relationship of any particular structural trait to physiological performance may be weak or undetectable. Furthermore, intraspecific variation in both structural and physiological traits leads to differences in plant size and fitness. These results demonstrate the importance of considering measurements of multivariate phenotypes on individual plants when evaluating trait relationships and how trait variation influences predictions of ecological and evolutionary outcomes.