Quantitative Genetics of Drosophila Melanogaster. II. Heritabilities and Genetic Correlations between Sexes for Head and Thorax Traits

A quantitative genetic analysis is reported for traits on the head and thorax of adult fruit flies, Drosophila melanogaster. Females are larger than males, and the magnitude of sexual dimorphism is similar for traits derived from the same imaginal disc, but the level of sexual dimorphism varies widely across discs. The greatest difference between males and females occurs for the dimensions of the sclerotized mouthparts of the proboscis. Most of the traits studied are highly heritable with heritabilities ranging from 0.26 to 0.84 for males and 0.27 to 0.81 for females. In general, heritabilities are slightly higher for males, possibly reflecting the effect of dosage compensation on X-linked variance. The X chromosome contributes substantially to variance for many of these traits, and including results reported elsewhere, the variance for over two-thirds of the traits studied includes X-linked variance. The genetic correlations between sexes for the same trait are generally high and close to unity. Coupled with the small differences in the traits between sexes for heritabilities and phenotypic variances, these results suggest that selection would be very slow to change the level of sexual dimorphism in size of various body parts.     

Multivariate selection and intersexual genetic constraints in a wild bird population

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra‐ and intersex additive genetic (co)variances and sex‐specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex‐specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex‐specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross‐sex genetic correlation = ?0.003, 95% CI = ?0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex‐specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.     

Sex differences in the genetic architecture of aggressiveness in a sexually dimorphic spider

Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.     

Genetic variation and plasticity of thorax length and wing length in Drosophila aldrichi and D. buzzatii

Reaction norms across three temperatures of development were measured for thorax length, wing length and wing length/thorax length ratio for ten isofemale lines from each of two populations of Drosophila aldrichi and D. buzzatii. Means for thorax and wing length in both species were larger at 24 °C than at either 18 °C or 31 °C, with the reduction in size at 18 °C most likely due to a nutritional constraint. Although females were larger than males, the sexes were not different for wing length/thorax length ratio. The plasticity of the traits differed between species and between populations of each species, with genetic variation in plasticity similar for the two species from one locality, but much higher for D. aldrichi from the other. Estimates of heritabilities for D. aldrichi generally were higher at 18 °C and 24 °C than at 31 °C, but for D. buzzatii they were highest at 31 °C, although heritabilities were not significantly different between species at any temperature. Additive genetic variances for D. aldrichi showed trends similar to that for heritability, being highest at 18 °C and decreasing as temperature increased. For D. buzzatii, however, additive genetic variances were lowest at 24 °C. These results are suggestive that genetic variation for body size characters is increased in more stressful environments. Thorax and wing lengths showed significant genetic correlations that were not different between the species, but the genetic correlations between each of these traits and their ratio were significantly different. For D. aldrichi, genetic variation in the wing length/thorax length ratio was due primarily to variation in thorax length, while for D. buzzatii, it was due primarily to variation in wing length. The wing length/thorax length ratio, which is the inverse of wing loading, decreased linearly as temperature increased, and it is suggested that this ratio may be of greater adaptive significance than either of its components.     

The genetic architecture of behavioral traits in a spider

The existence of consistent individual differences in behavior has been shown in a number of species, and several studies have found observable sex differences in these behaviors, yet their evolutionary implications remain unclear. Understanding the evolutionary dynamics of behavioral traits requires knowledge of their genetic architectures and whether this architecture differs between the sexes. We conducted a quantitative genetic study in a sexually size‐dimorphic spider, Larinioides sclopetarius, which exhibits sex differences in adult lifestyles. We observed pedigreed spiders for aggression, activity, exploration, and boldness and used animal models to disentangle genetic and environmental influences on these behaviors. We detected trends toward (i) higher additive genetic variances in aggression, activity, and exploration in males than females, and (ii) difference in variances due to common environment/maternal effects, permanent environment and residual variance in aggression and activity with the first two variances being higher in males for both behaviors. We found no sex differences in the amount of genetic and environmental variance in boldness. The mean heritability estimates of aggression, activity, exploration, and boldness range from 0.039 to 0.222 with no sizeable differences between females and males. We note that the credible intervals of the estimates are large, implying a high degree of uncertainty, which disallow a robust conclusion of sex differences in the quantitative genetic estimates. However, the observed estimates suggest that sex differences in the quantitative genetic architecture of the behaviors cannot be ruled out. Notably, the present study suggests that genetic underpinnings of behaviors may differ between sexes and it thus underscores the importance of taking sex differences into account in quantitative genetic studies.     

Genetics of Life History in DROSOPHILA MELANOGASTER. I. Sib Analysis of Adult Females

A sib analysis of adult life-history characters was performed on about twelve hundred females from a laboratory Drosophila melanogaster population that had been sampled from nature and cultured so as to preserve its genetic variability. The following results were found. There was no detectable trend with age in additive or dominance genetic variances for age-specific fecundity. Environmental variance for age-specific fecundity increased with age. The genetic variance for fecundity characters was primarily additive. The genetic variance for longevity was primarily dominance variance. There were negative genetic correlations between early fecundity and lifespan, as well as between mean egg-laying rate and longevity.     

Partitioning of genetic variation across the genome using multimarker methods in a wild bird population

The underlying basis of genetic variation in quantitative traits, in terms of the number of causal variants and the size of their effects, is largely unknown in natural populations. The expectation is that complex quantitative trait variation is attributable to many, possibly interacting, causal variants, whose effects may depend upon the sex, age and the environment in which they are expressed. A recently developed methodology in animal breeding derives a value of relatedness among individuals from high‐density genomic marker data, to estimate additive genetic variance within livestock populations. Here, we adapt and test the effectiveness of these methods to partition genetic variation for complex traits across genomic regions within ecological study populations where individuals have varying degrees of relatedness. We then apply this approach for the first time to a natural population and demonstrate that genetic variation in wing length in the great tit (Parus major) reflects contributions from multiple genomic regions. We show that a polygenic additive mode of gene action best describes the patterns observed, and we find no evidence of dosage compensation for the sex chromosome. Our results suggest that most of the genomic regions that influence wing length have the same effects in both sexes. We found a limited amount of genetic variance in males that is attributed to regions that have no effects in females, which could facilitate the sexual dimorphism observed for this trait. Although this exploratory work focuses on one complex trait, the methodology is generally applicable to any trait for any laboratory or wild population, paving the way for investigating sex‐, age‐ and environment‐specific genetic effects and thus the underlying genetic architecture of phenotype in biological study systems.     

The Nature of Quantitative Genetic Variation in Drosophila. III. Mechanism of Dosage Compensation for Sex-Linked Abdominal Bristle Polygenes

Seventeen lines, each homozygous for a different X chromosome but all with a common autosomal genetic background, were constructed and assayed for abdominal bristle number to determine whether dosage compensation operates for sex-linked genes affecting this character.—The regression coefficient of male mean on female mean using a logarithmic scale was 0.90 ± 0.13 and the genetic regression coefficient 0.92, neither differing significantly from unity. The genetic components of variance in males and females were also very similar (0.000234 or 0.000228, respectively). These results indicate that dosage compensation is complete (or nearly so) for sex-linked genes affecting this character. The bristle scores of females did not differ in reciprocal crosses between these lines, thus dosage compensation does not operate by paternal X inactivation.—The question of an adequate scale for abdominal bristle number had to be examined during the study. A logarithmic scale appeared to be adequate for both genotypic and environmental differences.     

THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of components of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental variability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by “good genes” models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations.     

Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep

Sexual conflict at loci influencing traits shared between the sexes occurs when sex-specific selection pressures are antagonistic relative to the genetic correlation between the sexes. To assess whether there is sexual conflict over shared traits, we estimated heritability and intersexual genetic correlations for highly sexually dimorphic traits (horn volume and body mass) in a wild population of bighorn sheep (Ovis canadensis) and quantified sex-specific selection using estimates of longevity and lifetime reproductive success. Body mass and horn volume showed significant additive genetic variance in both sexes, and intersexual genetic correlations were 0.24+/-0.28 for horn volume and 0.63+/-0.30 for body mass. For horn volume, selection coefficients did not significantly differ from zero in either sex. For body weight, selection coefficients were positive in females but did not differ from zero in males. The absence of detectable sexually antagonistic selection suggests that currently there are no sexual conflicts at loci influencing horn volume and body mass.     

Genetic Models for the Analysis of Data from the Families of Identical Twins

Genetic models are described which exploit the unique relationships that exist within the families of identical twins to obtain weighted least squares estimates of additive, dominance and epistatic components of genetic variance as well as estimates of the contributions of X-linked genes, maternal effects and three sources of environmental variation. Since all of the relationships required to achieve a resolution of these variance components are contained within each family unit, the model would appear to be superior to previous approaches to the analysis of quantitative traits in man.     

Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus)

Estimates of genetic components are important for our understanding of how individual characteristics are transferred between generations. We show that the level of heritability varies between 0.12 and 0.68 in six morphological traits in house sparrows (Passer domesticus L.) in northern Norway. Positive and negative genetic correlations were present among traits, suggesting evolutionary constraints on the evolution of some of these characters. A sexual difference in the amount of heritable genetic variation was found in tarsus length, wing length, bill depth and body condition index, with generally higher heritability in females. In addition, the structure of the genetic variance-covariance matrix for the traits differed between the sexes. Genetic correlations between males and females for the morphological traits were however large and not significantly different from one, indicating that sex-specific responses to selection will be influenced by intersexual differences in selection differentials. Despite this, some traits had heritability above 0.1 in females, even after conditioning on the additive genetic covariance between sexes and the additive genetic variances in males. Moreover, a meta-analysis indicated that higher heritability in females than in males may be common in birds. Thus, this indicates sexual differences in the genetic architecture of birds. Consequently, as in house sparrows, the evolutionary responses to selection will often be larger in females than males. Hence, our results suggest that sex-specific additive genetic variances and covariances, although ignored in most studies, should be included when making predictions of evolutionary changes from standard quantitative genetic models.     

EVOLVABILITY OF INDIVIDUAL TRAITS IN A MULTIVARIATE CONTEXT: PARTITIONING THE ADDITIVE GENETIC VARIANCE INTO COMMON AND SPECIFIC COMPONENTS

Genetic covariation among multiple traits will bias the direction of evolution. Although a trait's phenotypic context is crucial for understanding evolutionary constraints, the evolutionary potential of one (focal) trait, rather than the whole phenotype, is often of interest. The extent to which a focal trait can evolve independently depends on how much of the genetic variance in that trait is unique. Here, we present a hypothesis‐testing framework for estimating the genetic variance in a focal trait that is independent of variance in other traits. We illustrate our analytical approach using two Drosophila bunnanda trait sets: a contact pheromone system comprised of cuticular hydrocarbons (CHCs), and wing shape, characterized by relative warps of vein position coordinates. Only 9% of the additive genetic variation in CHCs was trait specific, suggesting individual traits are unlikely to evolve independently. In contrast, most (72%) of the additive genetic variance in wing shape was trait specific, suggesting relative warp representations of wing shape could evolve independently. The identification of genetic variance in focal traits that is independent of other traits provides a way of studying the evolvability of individual traits within the broader context of the multivariate phenotype.     

CHANGES IN THE HERITABILITY OF FIVE MORPHOLOGICAL TRAITS UNDER COMBINED ENVIRONMENTAL STRESSES IN DROSOPHILA MELANOGASTER

Heritabilities and evolvabilities for morphological traits were compared between two environments in Drosophila melanogaster using parent-offspring comparisons. One of the environments was favorable. The other stressful environment involved a combination of repeated cold shocks, poor nutrition, and ethanol added to the medium, which markedly decreased viability. For wing traits, heritabilities were relatively lower in the stressful environment, while heritabilities for bristle traits were not influenced by conditions. Heritability changes were largely due to an increase in the environmental variance under stress, whereas levels of additive genetic variance were relatively constant. Evolvabilities were similar between environments except for crossvein length.     

Age and sex affect quantitative genetic parameters for dominance rank and aggression in free‐living greylag geese

Knowledge of the genetic and environmental influences on a character is pivotal for understanding evolutionary changes in quantitative traits in natural populations. Dominance and aggression are ubiquitous traits that are selectively advantageous in many animal societies and have the potential to impact the evolutionary trajectory of animal populations. Here we provide age‐ and sex‐specific estimates of additive genetic and environmental components of variance for dominance rank and aggression rate in a free‐living, human‐habituated bird population subject to natural selection. We use a long‐term data set on individually marked greylag geese (Anser anser) and show that phenotypic variation in dominance‐related behaviours contains significant additive genetic variance, parental effects and permanent environment effects. The relative importance of these variance components varied between age and sex classes, whereby the most pronounced differences concerned nongenetic components. In particular, parental effects were larger in juveniles of both sexes than in adults. In paired adults, the partner's identity had a larger influence on male dominance rank and aggression rate than in females. In sex‐ and age‐specific estimates, heritabilities did not differ significantly between age and sex classes. Adult dominance rank was only weakly genetically correlated between the sexes, leading to considerably higher heritabilities in sex‐specific estimates than across sexes. We discuss these patterns in relation to selection acting on dominance rank and aggression in different life history stages and sexes and suggest that different adaptive optima could be a mechanism for maintaining genetic variation in dominance‐related traits in free‐living animal populations.     

High Stressful Temperature and Genetic Variation of Five Quantitative Traits in Drosophila Melanogaster

Variation of five quantitative traits (thorax length, wing length, sternopleural bristle number, developmental time and larva-to-adult viability) was studied in Drosophila melanogaster reared at standard (25°C) and high stressful (32°C) temperatures using half-sib analysis. In all traits, both phenotypic and environmental variances increased at 32°C. For genetic variances, only two statistically significant differences between temperature treatments were found: the among-sire variance of viability and the among-dam variance of developmental time were higher under stress. Among-sire genetic variances and evolvabilities were generally higher at 32°C but narrow sense heritabilities were not. The results of the present work considered in the context of other studies in D. melanogaster indicate different patterns of genetic variation between stressful and nonstressful environments for the traits examined. Data on thorax length and viability agree with the hypothesis that genetic variance can be increased under extreme environmental conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Cross‐sex genetic correlations and the evolution of sex‐specific local adaptation: Insights from classical trait clines in Drosophila melanogaster

Natural selection varies widely among locations of a species’ range, favoring population divergence and adaptation to local environmental conditions. Selection also differs between females and males, favoring the evolution of sexual dimorphism. Both forms of within‐species evolutionary diversification are widely studied, though largely in isolation, and it remains unclear whether environmental variability typically generates similar or distinct patterns of selection on each sex. Studies of sex‐specific local adaptation are also challenging because they must account for genetic correlations between female and male traits, which may lead to correlated patterns of trait divergence between sexes, whether or not local selection patterns are aligned or differ between the sexes. We quantified sex‐specific divergence in five clinally variable traits in Drosophila melanogaster that individually vary in their magnitude of cross‐sex genetic correlation (i.e., from moderate to strongly positive). In all five traits, we observed parallel male and female clines, regardless of the magnitude of their genetic correlation. These patterns imply that parallel spatial divergence of female and male traits is a reflection of sexually concordant directional selection imposed by local environmental conditions. In such contexts, genetic correlations between the sexes promote, rather than constrain, local adaptation to a spatially variable environment.     

Dosage Compensation in Drosophila: Evidence That daughterless and Sex-lethal Control X Chromosome Activity at the Blastoderm Stage of Embryogenesis

Dosage compensation is a mechanism that equalizes the expression of X chromosome linked genes in males, who have one X chromosome, with that in females, who have two. In Drosophila, this is achieved by the relative hyperactivation of X-linked genes in males, as was first shown by Muller using a phenotypic assay based on adult eye color. Several genes involved in regulating dosage compensation have been identified through the isolation of mutations that are sex-specific lethals. However, because of this lethality it is not straightforward to assay the relative roles of these genes using assays based on adult phenotypes. Here this problem is circumvented using an assay based on embryonic phenotypes. These experiments indicate that dosage compensation is established early in development and demonstrate that the daughterless and Sex-lethal gene products are involved in regulating X chromosome activity at the blastoderm stage of embryogenesis.