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.     

Natural selection and inheritance of breeding time and clutch size in the collared flycatcher

Many characteristics of organisms in free-living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often-cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long-term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation ("animal models") to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent-offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2 = 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA = -0.41 +/- 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (beta = -0.28 +/- 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (beta = -0.20 +/- 0.04), but not on clutch size (beta = 0.03 +/- 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life-history trade-offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life-history trade-offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.     

Measuring natural and sexual selection on breeding values of male display traits in Drosophila serrata

Fundamental to many theories of sexual selection is the expectation that sexual traits, which males use in an attempt to increase mating success, confer costs as well as benefits to individual males. Although evolution of exaggerated male traits is predicted to be halted, by costs applied by natural selection, there is a lack of empirical work devoted to quantitatively establishing whether natural selection opposes sexual selection generated by the preferences of females. In this study, we quantified natural and sexual selection gradients on breeding values for cuticular hydrocarbon (CHC) components of male contact pheromones in Drosophila serrata. As male sexual traits may often be environmentally condition dependent, breeding values were used in the selection analysis to remove the possibility of environmental correlations between the measured trait and fitness biasing estimates of selection. The direction of natural selection was found to oppose sexual selection on a subset of CHCs examined. Opposing natural and sexual selection suggests that further evolution of the male pheromone may in part be limited by costs associated with attractive male CHC blends.     

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called “paradox of stasis.” To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales.     

The genetic variance but not the genetic covariance of life‐history traits changes towards the north in a time‐constrained insect

Seasonal time constraints are usually stronger at higher than lower latitudes and can exert strong selection on life‐history traits and the correlations among these traits. To predict the response of life‐history traits to environmental change along a latitudinal gradient, information must be obtained about genetic variance in traits and also genetic correlation between traits, that is the genetic variance‐covariance matrix, G . Here, we estimated G for key life‐history traits in an obligate univoltine damselfly that faces seasonal time constraints. We exposed populations to simulated native temperatures and photoperiods and common garden environmental conditions in a laboratory set‐up. Despite differences in genetic variance in these traits between populations (lower variance at northern latitudes), there was no evidence for latitude‐specific covariance of the life‐history traits. At simulated native conditions, all populations showed strong genetic and phenotypic correlations between traits that shaped growth and development. The variance–covariance matrix changed considerably when populations were exposed to common garden conditions compared with the simulated natural conditions, showing the importance of environmentally induced changes in multivariate genetic structure. Our results highlight the importance of estimating variance–covariance matrixes in environments that mimic selection pressures and not only trait variances or mean trait values in common garden conditions for understanding the trait evolution across populations and environments.     

Response to joint selection on germination and flowering phenology depends on the direction of selection

Flowering and germination time are components of phenology, a complex phenotype that incorporates a number of traits. In natural populations, selection is likely to occur on multiple components of phenology at once. However, we have little knowledge of how joint selection on several phenological traits influences evolutionary response. We conducted one generation of artificial selection for all combinations of early and late germination and flowering on replicated lines within two independent base populations in the herb Campanula americana. We then measured response to selection and realized heritability for each trait. Response to selection and heritability were greater for flowering time than germination time, indicating greater evolutionary potential of this trait. Selection for earlier phenology, both flowering and germination, did not depend on the direction of selection on the other trait, whereas response to selection to delay germination and flowering was greater when selection on the other trait was in the opposite direction (e.g., early germination and late flowering), indicating a negative genetic correlation between the traits. Therefore, the extent to which correlations shaped response to selection depended on the direction of selection. Furthermore, the genetic correlation between timing of germination and flowering varies across the trait distributions. The negative correlation between germination and flowering time found when selecting for delayed phenology follows theoretical predictions of constraint for traits that jointly determine life history schedule. In contrast, the lack of constraint found when selecting for an accelerated phenology suggests a reduction of the covariance due to strong selection favoring earlier flowering and a shorter life cycle. This genetic architecture, in turn, will facilitate further evolution of the early phenology often favored in warm climates.     

Estimating selection on neonatal traits in red deer using elasticity path analysis

Van Tienderen recently published a method that links selection gradients between a phenotypic trait and multiple fitness components with the effects of these fitness components on the population growth rate (mean absolute fitness). The method allows selection to be simultaneously estimated across multiple fitness components in a population dynamic framework. In this paper we apply the method to a population of red deer living in the North Block of the Isle of Rum, Scotland. We show that (1) selection on birth date and birth weight can operate through multiple fitness components simultaneously; (2) our estimates of the response to selection are consistent with the observed change in trait values that we cannot explain with environmental and phenotypic covariates; (3) selection on both traits has fluctuated over the course of the study; (4) selection operates through different fitness components in different years; and (5) no environmental covariates correlate with selection because different fitness components respond to density and climatic variation in contrasting ways.     

Antler size in red deer: heritability and selection but no evolution

We present estimates of the selection on and the heritability of a male secondary sexual weapon in a wild population: antler size in red deer. Male red deer with large antlers had increased lifetime breeding success, both before and after correcting for body size, generating a standardized selection gradient of 0.44 (+/- 0.18 SE). Despite substantial age- and environment-related variation, antler size was also heritable (heritability of antler mass = 0.33 +/- 0.12). However the observed selection did not generate an evolutionary response in antler size over the study period of nearly 30 years, and there was no evidence of a positive genetic correlation between antler size and fitness nor of a positive association between breeding values for antler size and fitness. Our results are consistent with the hypothesis that a heritable trait under directional selection will not evolve if associations between the measured trait and fitness are determined by environmental covariances: In red deer males, for example, both antler size and success in the fights for mates may be heavily dependent on an individual's nutritional state.     

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.     

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.     

Temporal and genomic analysis of additive genetic variance in breeding programmes

Genetic variance is a central parameter in quantitative genetics and breeding. Assessing changes in genetic variance over time as well as the genome is therefore of high interest. Here, we extend a previously proposed framework for temporal analysis of genetic variance using the pedigree-based model, to a new framework for temporal and genomic analysis of genetic variance using marker-based models. To this end, we describe the theory of partitioning genetic variance into genic variance and within-chromosome and between-chromosome linkage-disequilibrium, and how to estimate these variance components from a marker-based model fitted to observed phenotype and marker data. The new framework involves three steps: (i) fitting a marker-based model to data, (ii) sampling realisations of marker effects from the fitted model and for each sample calculating realisations of genetic values and (iii) calculating the variance of sampled genetic values by time and genome partitions. Analysing time partitions indicates breeding programme sustainability, while analysing genome partitions indicates contributions from chromosomes and chromosome pairs and linkage-disequilibrium. We demonstrate the framework with a simulated breeding programme involving a complex trait. Results show good concordance between simulated and estimated variances, provided that the fitted model is capturing genetic complexity of a trait. We observe a reduction of genetic variance due to selection and drift changing allele frequencies, and due to selection inducing negative linkage-disequilibrium.Subject terms: Genetic variation, Quantitative trait, Agricultural genetics, Plant breeding, Agriculture     

Evolution of genetic variation for selected traits in successive breeding populations of maritime pine

Directional selection impacts a trait distribution by shifting its mean and reducing its variance. The change of variance is of major importance as the response to selection in subsequent generations is highly dependent of the genetic variability available in the population. In this contribution, evolution of genetic variation was investigated through the first breeding populations of the French maritime pine (Pinus pinaster Ait.) breeding program. We considered three populations: P0 (the forest where plus trees were initially selected), G0 (the plus tree population) and G1 (the population composed of trees selected in the progenies of G0). Analyses focused on the following selected traits: total height (H), girth at 1.30 m (D) and stem deviation to verticality (S). More than 150,000 trees from 25 tests of three distinct populations were studied with an individual genetic model. Accurate genetic parameters were obtained by taking all relationships between trees into account. For H and D, we found a strong decrease of the genetic variation from P0 to G0 corresponding to the initial selection of plus trees, which constitutes the base population of the breeding program. Then, despite the second step of selection applied, no appreciable evolution arose from comparisons between G0 and G1 for these traits. For S, the evolution is less significant as phenotypic variation slightly increased, possibly due to changes of silvicultural practices.     

Good genes and old age: Do old mates provide superior genes?

It has been suggested that female preference for older mates in species without parental care has evolved in response to an alleged higher genetic quality of older individuals. This is based on the widespread assumption that viability selection produces older individuals that are genetically superior to younger individuals. In contrast, we propose that the oldest individuals rarely are genetically superior. Quantitative genetic models of life history evolution indicate that young to intermediately aged individuals are likely to possess the highest breeding values of fitness. This conclusion is based on four arguments: 1) Viability selection on older individuals may decrease or at least not substantially increase breeding values of fitness, because there may exist negative genetic correlations between late-age and early-age life history parameters, 2) Fertility selection is likely to raise the fitness of gametes produced by young individuals more than those produced by old individuals, because the covariance between fertility and fitness often decreases with age, 3) The history of selection on their parents makes younger individuals more fit than older individuals, 4) Germ-line mutations, which are generally deleterious, significantly decrease the breeding value of fitness of an individual throughout its lifespan, especially in males. Therefore, females that mate with the oldest males in a population are doing so for reasons other than to obtain offspring of high genetic quality.     

Genetic variation and co-variation for fitness between intra-population and inter-population backgrounds in the red flour beetle, Tribolium castaneum

Hybrids from crosses between populations of the flour beetle, Tribolium castaneum, express varying degrees of inviability and morphological abnormalities. The proportion of allopatric population hybrids exhibiting these negative hybrid phenotypes varies widely, from 3% to 100%, depending upon the pair of populations crossed. We crossed three populations and measured two fitness components, fertility and adult offspring numbers from successful crosses, to determine how genes segregating within populations interact in inter-population hybrids to cause the negative phenotypes. With data from crosses of 40 sires from each of three populations to groups of five dams from their own and two divergent populations, we estimated the genetic variance and covariance for breeding value of fitness between the intra- and inter-population backgrounds and the sire × dam population interaction variance. The latter component of the variance in breeding values estimates the change in genic effects between backgrounds owing to epistasis. Interacting genes with a positive effect, prior to fixation, in the sympatric background but a negative effect in the hybrid background cause reproductive incompatibility in the Dobzhansky-Muller speciation model. Thus, the sire × dam population interaction provides a way to measure the progress towards speciation of genetically differentiating populations on a trait by trait basis using inter-population hybrids.     

Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird

Indirect and direct models of sexual selection make different predictions regarding the quantitative genetic relationships between sexual ornaments and fitness. Indirect models predict that ornaments should have a high heritability and that strong positive genetic covariance should exist between fitness and the ornament. Direct models, on the other hand, make no such assumptions about the level of genetic variance in fitness and the ornament, and are therefore likely to be more important when environmental sources of variation are large. Here we test these predictions in a wild population of the blue tit (Parus caeruleus), a species in which plumage coloration has been shown to be under sexual selection. Using 3 years of cross-fostering data from over 250 breeding attempts, we partition the covariance between parental coloration and aspects of nestling fitness into a genetic and environmental component. Contrary to indirect models of sexual selection, but in agreement with direct models, we show that variation in coloration is only weakly heritable h2<0.11, and that two components of offspring fitness-nestling size and fledgling recruitment-are strongly dependent on parental effects, rather than genetic effects. Furthermore, there was no evidence of significant positive genetic covariation between parental colour and offspring traits. Contrary to direct benefit models, however, we find little evidence that variation in colour reliably indicates the level of parental care provided by either males or females. Taken together, these results indicate that the assumptions of indirect models of sexual selection are not supported by the genetic basis of the traits reported on here.     

Mapping quantitative trait loci in selected breeding populations: A segregation distortion approach

Quantitative trait locus (QTL) mapping is often conducted in line-crossing experiments where a sample of individuals is randomly selected from a pool of all potential progeny. QTLs detected from such an experiment are important for us to understand the genetic mechanisms governing a complex trait, but may not be directly relevant to plant breeding if they are not detected from the breeding population where selection is targeting for. QTLs segregating in one population may not necessarily segregate in another population. To facilitate marker-assisted selection, QTLs must be detected from the very population which the selection is targeting. However, selected breeding populations often have depleted genetic variation with small population sizes, resulting in low power in detecting useful QTLs. On the other hand, if selection is effective, loci controlling the selected trait will deviate from the expected Mendelian segregation ratio. In this study, we proposed to detect QTLs in selected breeding populations via the detection of marker segregation distortion in either a single population or multiple populations using the same selection scheme. Simulation studies showed that QTL can be detected in strong selected populations with selected population sizes as small as 25 plants. We applied the new method to detect QTLs in two breeding populations of rice selected for high grain yield. Seven QTLs were identified, four of which have been validated in advanced generations in a follow-up study. Cloned genes in the vicinity of the four QTLs were also reported in the literatures. This mapping-by-selection approach provides a new avenue for breeders to improve breeding progress. The new method can be applied to breeding programs not only in rice but also in other agricultural species including crops, trees and animals.     

The impact of recombination on short-term selection gain in plant breeding experiments

Recombination is a requirement for response to selection, but researchers still debate whether increasing recombination beyond normal levels will result in significant gains in short-term selection. We tested this hypothesis, in the context of plant breeding, through a series of simulation experiments comparing short-term selection response (≤20 cycles) between populations with normal levels of recombination and similar populations with unconstrained recombination (i.e., free recombination). We considered additive and epistatic models and examined a wide range of values for key design variables: selection cycles, QTL number, heritability, linkage phase, selection intensity and population size. With few exceptions, going from normal to unconstrained levels of recombination produced only modest gains in response to selection (≈11 % on average). We then asked how breeders might capture some of this theoretical gain by increasing recombination through either (1) extra rounds of mating or (2) selection of highly recombinant individuals via use of molecular markers/maps. All methods tested captured less than half of the potential gain, but our analysis indicates that the most effective method is to select for increased recombination and the trait simultaneously. This recommendation is based on evidence of a favorable interaction between trait selection and the impact of recombination on selection gains. Finally, we examined the relative contributions of the two components of meiotic recombination, chromosome assortment and crossing over, to short-term selection gain. Depending primarily on the presence of trait selection pressure, chromosome assortment alone accounted for 40–75 % of gain in response to short-term selection.     

Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance‐covariance matrix, G , determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance‐covariance matrix ( P ) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P , suggesting that natural selection may have influenced the evolution of genetic constraint in this species.     

Quantification and decomposition of environment‐selection relationships

In nature, selection varies across time in most environments, but we lack an understanding of how specific ecological changes drive this variation. Ecological factors can alter phenotypic selection coefficients through changes in trait distributions or individual mean fitness, even when the trait‐absolute fitness relationship remains constant. We apply and extend a regression‐based approach in a population of Soay sheep (Ovis aries) and suggest metrics of environment‐selection relationships that can be compared across studies. We then introduce a novel method that constructs an environmentally structured fitness function. This allows calculation of full (as in existing approaches) and partial (acting separately through the absolute fitness function slope, mean fitness, and phenotype distribution) sensitivities of selection to an ecological variable. Both approaches show positive overall effects of density on viability selection of lamb mass. However, the second approach demonstrates that this relationship is largely driven by effects of density on mean fitness, rather than on the trait‐fitness relationship slope. If such mechanisms of environmental dependence of selection are common, this could have important implications regarding the frequency of fluctuating selection, and how previous selection inferences relate to longer term evolutionary dynamics.     

Predicted accuracy of and response to genomic selection for new traits in dairy cattle

Genomic selection relaxes the requirement of traditional selection tools to have phenotypic measurements on close relatives of all selection candidates. This opens up possibilities to select for traits that are difficult or expensive to measure. The objectives of this paper were to predict accuracy of and response to genomic selection for a new trait, considering that only a cow reference population of moderate size was available for the new trait, and that selection simultaneously targeted an index and this new trait. Accuracy for and response to selection were deterministically evaluated for three different breeding goals. Single trait selection for the new trait based only on a limited cow reference population of up to 10 000 cows, showed that maximum genetic responses of 0.20 and 0.28 genetic standard deviation (s.d.) per year can be achieved for traits with a heritability of 0.05 and 0.30, respectively. Adding information from the index based on a reference population of 5000 bulls, and assuming a genetic correlation of 0.5, increased genetic response for both heritability levels by up to 0.14 genetic s.d. per year. The scenario with simultaneous selection for the new trait and the index, yielded a substantially lower response for the new trait, especially when the genetic correlation with the index was negative. Despite the lower response for the index, whenever the new trait had considerable economic value, including the cow reference population considerably improved the genetic response for the new trait. For scenarios with a zero or negative genetic correlation with the index and equal economic value for the index and the new trait, a reference population of 2000 cows increased genetic response for the new trait with at least 0.10 and 0.20 genetic s.d. per year, for heritability levels of 0.05 and 0.30, respectively. We conclude that for new traits with a very small or positive genetic correlation with the index, and a high positive economic value, considerable genetic response can already be achieved based on a cow reference population with only 2000 records, even when the reliability of individual genomic breeding values is much lower than currently accepted in dairy cattle breeding programs. New traits may generally have a negative genetic correlation with the index and a small positive economic value. For such new traits, cow reference populations of at least 10 000 cows may be required to achieve acceptable levels of genetic response for the new trait and for the whole breeding goal.