The effect of non-additive genetic interactions on selection in multi-locus genetic models

Additive genetic variance might usually be expected to decrease in a finite population because of genetic drift. However, both theoretical and empirical studies have shown that the additive genetic variance of a population could, in some cases, actually increase owing to the action of genetic drift in presence of non-additive effects. We used Monte-Carlo simulations to address a less-well-studied issue: the effects of directional truncation selection on a trait affected by non-additive genetic variation. We investigated the effects on genetic variance and the response to selection. We compared two different genetic models, representing various numbers of loci. We found that the additive genetic variance could also increase in the case of truncation selection, when dominance and epistasis was present. Additive-by-additive epistatic effects generally gave a higher increase in additive variance compared to dominance. However, the magnitude of the increase differed depending on the particular model and on the number of loci.     

Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster

For insects, temperature is a major environmental variable that can influence an individual's behavioral activities and fitness. Drosophila melanogaster is a cosmopolitan species that has had great success in adapting to and colonizing diverse thermal niches. This adaptation and colonization has resulted in complex patterns of genetic variation in thermotolerance phenotypes in nature. Although extensive work has been conducted documenting patterns of genetic variation, substantially less is known about the genomic regions or genes that underlie this ecologically and evolutionarily important genetic variation. To begin to understand and identify the genes controlling thermotolerance phenotypes, we have used a mapping population of recombinant inbred (RI) lines to map quantitative trait loci (QTL) that affect variation in both heat- and cold-stress resistance. The mapping population was derived from a cross between two lines of D. melanogaster (Oregon-R and 2b) that were not selected for thermotolerance phenotypes, but exhibit significant genetic divergence for both phenotypes. Using a design in which each RI line was backcrossed to both parental lines, we mapped seven QTL affecting thermotolerance on the second and third chromosomes. Three of the QTL influence cold-stress resistance and four affect heat-stress resistance. Most of the QTL were trait or sex specific, suggesting that overlapping but generally unique genetic architectures underlie resistance to low- and high-temperature extremes. Each QTL explained between 5 and 14% of the genetic variance among lines, and degrees of dominance ranged from completely additive to partial dominance. Potential thermotolerance candidate loci contained within our QTL regions are identified and discussed.     

Genetics of tassel branch number in maize and its implications for a selection program for small tassel size

Summary Tassel branch numbers of six crosses of maize (Zea mays L.) were analyzed to determine inheritance of this trait. Generation mean analyses were used to estimate genetic effects, and additive and nonadditive components of variance were calculated and evaluated for bias due to linkage. Both narrow-sense and broad-sense heritabilities were estimated. Additive genetic variance estimates were significant in five of the six crosses, whereas estimates of variance due to nonadditive components were significant in only three crosses. Additionally, estimates of additive variance components usually were larger than corresponding nonadditive components. There was no evidence for linkage bias in these estimates. Estimates of additive genetic effects were significant in four of six crosses, but significant dominance, additive × additive and additive × dominance effects also were detected. Additive, dominance, and epistatic gene action, therefore, all influenced the inheritance of tassel branch number, but additive gene action was most important. Both narrow-sense and broadsense heritability estimates were larger than those reported for other physiological traits of maize and corroborated conclusions concerning the importance of additive gene action inferred from analyses of genetic effects and variances. We concluded that selection for smalltasseled inbreds could be accomplished most easily through a mass-selection and/or pedigree-selection system. Production of a small-tasseled hybrid would require crossing of two small-tasseled inbreds. We proposed two genetic models to explain unexpected results obtained for two crosses. One model involved five interacting loci and the other employed two loci displaying only additive and additive × additive gene action.Journal Paper No. J-9231 of the Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa 50011. Project No. 2152     

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.     

Phenotypic plasticity for life-history traits in Drosophila melanogaster. III. Effect of the environment on genetic parameters.

We estimated genetic and environmental variance components for developmental time and dry weight at eclosion in Drosophila melanogaster raised in ten different environments (all combinations of 22, 25 and 28 degrees C and 0.5, 1 and 4% yeast concentration, and 0.25% yeast at 25 degrees C). We used six homozygous lines derived from a natural population for complete diallel crosses in each environment. Additive genetic variances were consistently low for both traits (h2 around 10%). The additive genetic variance of developmental time was larger at lower yeast concentrations, but the heritability did not increase because other components were also larger. The additive genetic effects of the six parental lines changed ranks across environments, suggesting a mechanism for the maintenance of genetic variation in heterogenous environments. The variance due to non-directional dominance was small in most environments. However, there was directional dominance in the form of inbreeding depression for both traits. It was pronounced at high yeast levels and temperatures but disappeared when yeast or temperature were decreased. This meant that the heterozygous flies were more sensitive to environmental differences than homozygous flies. Because dominance effects are not heritable, this suggests that the evolution of plasticity can be constrained when dominance effects are important as a mechanism for plasticity.     

Variations in morphological and life-history traits under extreme temperatures in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

Using half-sib analysis, we analysed the consequences of extreme rearing temperatures on genetic and phenotypic variations in the morphological and life-history traits of Drosophila ananassae. Paternal half-sib covariance contains a relatively small proportion of the epistatic variance and lacks the dominance variance and variance due to maternal effect, which provides more reliable estimates of additive genetic variance. Experiments were performed on a mass culture population of D. ananassae collected from Kanniyakumari (India). Two extremely stressful temperatures (18°C and 32°C) and one standard temperature (25°C) were used to examine the effect of stressful and non-stressful environments on the morphological and life-history traits in males and females. Mean values of various morphological traits differed significantly among different temperature regimens in both males and females. Rearing at 18°C and 32°C resulted in decreased thorax length, wing-to-thorax (w/t) ratio, sternopleural bristle number, ovariole number, sex comb-tooth number and testis length. Phenotypic variances increased under stressful temperatures in comparison with non-stressful temperatures. Heritability and evolvability based on among-sires (males), among-dams (females), and the sum of the two components (sire + dam) showed higher values at both the stressful temperatures than at the non-stressful temperature. These differences reflect changes in additive genetic variance. Viability was greater at the high than the low extreme temperature. As viability is an indicator of stress, we can assume that stress was greater at 18°C than at 32°C in D. ananassae. The genetic variations for all the quantitative and life-history traits were higher at low temperature. Variation in sexual traits was more pronounced as compared with other morphometric traits, which shows that sexual traits are more prone to thermal stress. Our results agree with the hypothesis that genetic variation is increased in stressful environments.     

Maintenance of genetic variation in quantitative traits of a woodland rodent during generations of captive breeding

Breeding programs to conserve diversity are predicated on the assumption that genetic variation in adaptively important traits will be lost in parallel to the loss of variation at neutral loci. To test this assumption, we monitored quantitative traits across 18 generations of Peromyscus leucopus mice propagated with protocols that mirror breeding programs for threatened species. Ears, hind feet, and tails became shorter, but changes were reversible by outcrossing and therefore were due to accumulated inbreeding. Heritability of ear length decreased, because of an increase in phenotypic variance rather than the expected decrease in additive genetic variance. Additive genetic variance in hind foot length increased. This trait initially had low heritability but large dominance or common environmental variance contributing to resemblance among full-sibs. The increase in the additive component indicates that there was conversion of interaction variances to additive variance. For no trait did additive genetic variation decrease significantly across generations. These findings indicate that the restructuring of genetic variance that occurs with genetic drift and novel selection in captivity can prevent or delay the loss of phenotypic and heritable variation, providing variation on which selection can act to adapt populations to captivity and perhaps later to readapt to more natural habitats after release. Therefore, the importance of minimizing loss of gene diversity from conservation breeding programs for threatened wildlife species might lie in preventing immediate reduction in individual fitness due to inbreeding and protecting allelic diversity for long-term evolutionary change, more so than in protecting variation in quantitative traits for rapid re-adaptation to wild environments.     

The Effect of an Experimental Bottleneck upon Quantitative Genetic Variation in the Housefly

Effects of a population bottleneck (founder-flush cycle) upon quantitative genetic variation of morphometric traits were examined in replicated experimental lines of the housefly founded with one, four or 16 pairs of flies. Heritability and additive genetic variances for eight morphometric traits generally increased as a result of the bottleneck, but the pattern of increase among bottleneck sizes differed among traits. Principal axes of the additive genetic correlation matrix for the control line yielded two suites of traits, one associated with general body size and another set largely independent of body size. In the former set containing five of the traits, additive genetic variance was greatest in the bottleneck size of four pairs, whereas in the latter set of two traits the largest additive genetic variance occurred in the smallest bottleneck size of one pair. One trait exhibited changes in additive genetic variance intermediate between these two major responses. These results were inconsistent with models of additive effects of alleles within loci or of additive effects among loci. An observed decline in viability measures and body size in the bottleneck lines also indicated that there was nonadditivity of allelic effects for these traits. Several possible nonadditive models were explored that increased additive genetic variance as a result of a bottleneck. These included a model with complete dominance, a model with overdominance and a model incorporating multiplicative epistasis.     

Quantitative genetic analysis of the body size and shape of Drosophila buzzatii

Summary Body size in Drosophila is known to be closely related to a number of traits with important life history consequences, such as fecundity, dispersal ability and mating success. We examine the quantitative genetic basis of body size in three populations of the cactophilic species Drosophila buzzatii, which inhabit climatically different areas of Australia. Flies were reared individually to eliminate any common environmental component in a full-sib design with families split between two temperatures (18° and 25 °C). The means of several size measures differ significantly among populations while the genetic correlations among these traits generally do not differ, either among populations from different natural environments or between the different laboratory temperatures. This stability of correlation structure is necessary if laboratory estimates of genetic correlations are to have any connection with the expression of genetic variation in the field. The amount of variance due to genotype-by-environment interactions (family x temperature of development) varied among populations, apparently in parallel with the magnitudes of seasonal and diurnal variation in temperature experienced by the different populations. A coastal population, inhabiting a relatively thermally benign environment, showed no interaction, while two inland populations, inhabiting thermally more extreme areas, showed interaction. This interaction term is a measure of the amount of genetic variation in the degree of phenotypic plasticity of body size in response to temperature of development. Thus the inland flies vary in their ability to attain a given body size at a particular temperature while the coastal flies do not. This phenotypic plasticity is shown to be due primarily to differences among genotypes in the amount of response to the change in temperature. A possible selective basis for the maintenance of genetic variation for the levels of phenotypic plasticity is proposed.     

Cross prediction studies on spring barley

Summary Additive genetic, dominance genetic and environmental correlations between pairs of agronomically important characters in five spring barley crosses were calculated from estimates of the components of variance and covariance, obtained by Triple Test Cross analysis. Phenotypic correlations were calculated from the Triple Test Cross family means and compared to the additive genetic correlations. Phenotypic correlations were generally lower than the additive genetic correlations and, occasionally, of different sign. The highest phenotypic correlations between single plant yield and its components were found with number of tillers whereas these were the lowest additive genetic correlations, thousand grain weight giving the highest. High dominance genetic correlations were found between single plant yield and both grain number and thousand grain weight thus indirect early generation selection for single plant yield using these two characters would be ineffective. Additive and dominance genetic correlations confirm association of the erectoides dwarfing gene with low thousand grain weight and plant yield.     

Improvement of Prediction Ability for Genomic Selection of Dairy Cattle by Including Dominance Effects

Dominance may be an important source of non-additive genetic variance for many traits of dairy cattle. However, nearly all prediction models for dairy cattle have included only additive effects because of the limited number of cows with both genotypes and phenotypes. The role of dominance in the Holstein and Jersey breeds was investigated for eight traits: milk, fat, and protein yields; productive life; daughter pregnancy rate; somatic cell score; fat percent and protein percent. Additive and dominance variance components were estimated and then used to estimate additive and dominance effects of single nucleotide polymorphisms (SNPs). The predictive abilities of three models with both additive and dominance effects and a model with additive effects only were assessed using ten-fold cross-validation. One procedure estimated dominance values, and another estimated dominance deviations; calculation of the dominance relationship matrix was different for the two methods. The third approach enlarged the dataset by including cows with genotype probabilities derived using genotyped ancestors. For yield traits, dominance variance accounted for 5 and 7% of total variance for Holsteins and Jerseys, respectively; using dominance deviations resulted in smaller dominance and larger additive variance estimates. For non-yield traits, dominance variances were very small for both breeds. For yield traits, including additive and dominance effects fit the data better than including only additive effects; average correlations between estimated genetic effects and phenotypes showed that prediction accuracy increased when both effects rather than just additive effects were included. No corresponding gains in prediction ability were found for non-yield traits. Including cows with derived genotype probabilities from genotyped ancestors did not improve prediction accuracy. The largest additive effects were located on chromosome 14 near DGAT1 for yield traits for both breeds; those SNPs also showed the largest dominance effects for fat yield (both breeds) as well as for Holstein milk yield.     

Inheritance of partial resistance to powdery mildew in spring wheat

Summary Four spring wheat (Triticum aestivum L.) cultivars exhibiting partial resistance to powdery mildew induced by Erysiphe graminis f.sp. tritici were crossed to a common susceptible cultivar to study the inheritance of resistance. The genetic parameters contributing to resistance were estimated by generation means analyses. Additive gene action was the most important genetic component of variation among generation means in all four crosses. Additive by additive effects were significant in one cross and both additive by additive and additive by dominance effects were significant in another. Dominance effects were not significant. The F2/F3 correlations in three crosses ranged from 0.27 to 0.43. Three additional crosses among resistant cultivars were employed to study the effectiveness of selection in improving resistance. By selecting the most resistant plants from the F2 and evaluating the progenies in the F4, increases in resistance ranging from 21% to 31% were obtained. In all crosses, there was transgressive segregation in both directions indicating that the genes conferring resistance to these cultivars differ and exhibit additive effects.     

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.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

Evolution of additive and nonadditive genetic variance in development time along a cline in Drosophila serrata

Abstract. Latitudinal clines provide natural systems that may allow the effect of natural selection on the genetic variance to be determined. Ten clinal populations of Drosophila serrata collected from the eastern coast of Australia were used to examine clinal patterns in the trait mean and genetic variance of the life-history trait egg-to-adult development time. Development time significantly lengthened from tropical areas to temperate areas. The additive genetic variance for development time in each population was not associated with latitude but was associated with the population mean development time. Additive genetic variance tended to be larger in populations with more extreme development times and appeared to be consistent with allele frequency change. In contrast, the nonadditive genetic variance was not associated with the population mean but was associated with latitude. Levels of nonadditive genetic variance were greatest in the region of the cline where the gradient in the change in mean was greatest, consistent with Barton's (1999) conjecture that the generation of linkage disequilibrium may become an important component of the genetic variance in systems with a spatially varying optimum.     

THE HERITABLE BASIS OF VARIATION IN LARVAL DEVELOPMENTAL PATTERNS WITHIN POPULATIONS OF THE WOOD FROG (RANA SYLVATICA)

This study compares the heritable basis of variation in larval developmental patterns of mountain and lowland populations of the wood frog, Rana sylvatica. Additive genetic variances, heritabilities, and genetic correlations for larval developmental time and size at metamorphosis are estimated from half-sib and full-sib crosses. Considerable additive-genetic variances and high heritabilities are revealed for developmental time in both the mountain and the lowland population. There was a high level of additive-genetic variance and high heritability for body size at metamorphosis in the mountain population, but these were very low in the lowland population. The genetic correlations between developmental rate and larval body size are negative for the mountain population and near zero for the lowland population. It is argued that the differences in genetic structure between these two populations reflect differences in the selective regimes of their respective environments.     

Dissecting total genetic variance into additive and dominance components of purebred and crossbred pig traits

The partition of the total genetic variance into its additive and non-additive components can differ from trait to trait, and between purebred and crossbred populations. A quantification of these genetic variance components will determine the extent to which it would be of interest to account for dominance in genomic evaluations or to establish mate allocation strategies along different populations and traits. This study aims at assessing the contribution of the additive and dominance genomic variances to the phenotype expression of several purebred Piétrain and crossbred (Piétrain × Large White) pig performances. A total of 636 purebred and 720 crossbred male piglets were phenotyped for 22 traits that can be classified into six groups of traits: growth rate and feed efficiency, carcass composition, meat quality, behaviour, boar taint and puberty. Additive and dominance variances estimated in univariate genotypic models, including additive and dominance genotypic effects, and a genomic inbreeding covariate allowed to retrieve the additive and dominance single nucleotide polymorphism variances for purebred and crossbred performances. These estimated variances were used, together with the allelic frequencies of the parental populations, to obtain additive and dominance variances in terms of genetic breeding values and dominance deviations. Estimates of the Piétrain and Large White allelic contributions to the crossbred variance were of about the same magnitude in all the traits. Estimates of additive genetic variances were similar regardless of the inclusion of dominance. Some traits showed relevant amount of dominance genetic variance with respect to phenotypic variance in both populations (i.e. growth rate 8%, feed conversion ratio 9% to 12%, backfat thickness 14% to 12%, purebreds-crossbreds). Other traits showed higher amount in crossbreds (i.e. ham cut 8% to 13%, loin 7% to 16%, pH semimembranosus 13% to 18%, pH longissimus dorsi 9% to 14%, androstenone 5% to 13% and estradiol 6% to 11%, purebreds-crossbreds). It was not encountered a clear common pattern of dominance expression between groups of analysed traits and between populations. These estimates give initial hints regarding which traits could benefit from accounting for dominance for example to improve genomic estimated breeding value accuracy in genetic evaluations or to boost the total genetic value of progeny by means of assortative mating.     

Effect on linkage disequilibrium of selection for a quantitative character with epistasis

Summary Selection for a character controlled by additive genes induces linkage disequilibrium which reduces the additive genetic variance usable for further selective gains. Additive x additive epistasis contributes to selection response through development of linkage disequilibrium between interacting loci. To investigate the relative importance of the two effects of linkage disequilibrium, formulae are presented and results are reported of simulations using models involving additive, additive x additive and dominance components. The results suggest that so long as epistatic effects are not large relative to additive effects, and the proportion of pairs of loci which show epistasis is not very high, the predominant effect of linkage disequilibrium will be to reduce the rate of selection response.     

Genomic analysis of dominance effects on milk production and conformation traits in Fleckvieh cattle

Background

Estimates of dominance variance in dairy cattle based on pedigree data vary considerably across traits and amount to up to 50% of the total genetic variance for conformation traits and up to 43% for milk production traits. Using bovine SNP (single nucleotide polymorphism) genotypes, dominance variance can be estimated both at the marker level and at the animal level using genomic dominance effect relationship matrices. Yield deviations of high-density genotyped Fleckvieh cows were used to assess cross-validation accuracy of genomic predictions with additive and dominance models. The potential use of dominance variance in planned matings was also investigated.

Results

Variance components of nine milk production and conformation traits were estimated with additive and dominance models using yield deviations of 1996 Fleckvieh cows and ranged from 3.3% to 50.5% of the total genetic variance. REML and Gibbs sampling estimates showed good concordance. Although standard errors of estimates of dominance variance were rather large, estimates of dominance variance for milk, fat and protein yields, somatic cell score and milkability were significantly different from 0. Cross-validation accuracy of predicted breeding values was higher with genomic models than with the pedigree model. Inclusion of dominance effects did not increase the accuracy of the predicted breeding and total genetic values. Additive and dominance SNP effects for milk yield and protein yield were estimated with a BLUP (best linear unbiased prediction) model and used to calculate expectations of breeding values and total genetic values for putative offspring. Selection on total genetic value instead of breeding value would result in a larger expected total genetic superiority in progeny, i.e. 14.8% for milk yield and 27.8% for protein yield and reduce the expected additive genetic gain only by 4.5% for milk yield and 2.6% for protein yield.

Conclusions

Estimated dominance variance was substantial for most of the analyzed traits. Due to small dominance effect relationships between cows, predictions of individual dominance deviations were very inaccurate and including dominance in the model did not improve prediction accuracy in the cross-validation study. Exploitation of dominance variance in assortative matings was promising and did not appear to severely compromise additive genetic gain.     

Alternative life histories in the Atlantic salmon: genetic covariances within the sneaker sexual tactic in males

Alternative reproductive tactics are ubiquitous in many species. Tactic expression often depends on whether an individual's condition surpasses thresholds that are responsible for activating particular developmental pathways. Two central goals in understanding the evolution of reproductive tactics are quantifying the extent to which thresholds are explained by additive genetic effects, and describing their covariation with condition-related traits. We monitored the development of early sexual maturation that leads to the sneaker reproductive tactic in Atlantic salmon (Salmo salar L.). We found evidence for additive genetic variance in the timing of sexual maturity (which is a measure of the surpassing of threshold values) and body-size traits. This suggests that selection can affect the patterns of sexual development by changing the timing of this event and/or body size. Significant levels of covariation between these traits also occurred, implying a potential for correlated responses to selection. Closer examination of genetic covariances suggests that the detected genetic variation is distributed along at least five directions of phenotypic variation. Our results show that the potential for evolution of the life-history traits constituting this reproductive phenotype is greatly influenced by their patterns of genetic covariance.