Distinguishing adaptive from nonadaptive genetic differentiation: comparison of Q(ST) and F(ST) at two spatial scales

Genetic differentiation in 20 hierarchically sampled populations of wild barley was analyzed with quantitative traits, allozymes and Random Amplified Polymorphic DNAs (RAPDs), and compared for three marker types at two hierarchical levels. Regional subdivision for both molecular markers was much lower than for quantitative traits. For both allozymes and RAPDs, most loci exhibited minor or no regional differentiation, and the relatively high overall estimates of the latter were due to several loci with exceptionally high regional differentiation. The allozyme- and RAPD-specific patterns of differentiation were concordant in general with one another, but not with quantitative trait differentiation. Divergent selection on quantitative traits inferred from very high regional Q(ST) was in full agreement with our previous results obtained from a test of local adaptation and multilevel selection analysis. In contrast, most variation in allozyme and RAPD variation was neutral, although several allozyme loci and RAPD markers were exceptional in their levels of regional differentiation. However, it is not possible to answer the question whether these exceptional loci are directly involved in the response to selection pressure or merely linked to the selected loci. The fact that Q(ST) and F(ST) did not differ at the population scale, that is, within regions, but differed at the regional scale, for which local adaptation has been previously shown, implies that comparison of the level of subdivision in quantitative traits, as compared with molecular markers, is indicative of adaptive population differentiation only when sampling is carried out at the appropriate scale.     

Adaptive differentiation of quantitative traits in the globally distributed weed, wild radish (Raphanus raphanistrum)

Weedy species with wide geographical distributions may face strong selection to adapt to new environments, which can lead to adaptive genetic differentiation among populations. However, genetic drift, particularly due to founder effects, will also commonly result in differentiation in colonizing species. To test whether selection has contributed to trait divergence, we compared differentiation at eight microsatellite loci (measured as F(ST)) to differentiation of quantitative floral and phenological traits (measured as Q(ST)) of wild radish (Raphanus raphanistrum) across populations from three continents. We sampled eight populations: seven naturalized populations and one from its native range. By comparing estimates of Q(ST) and F(ST), we found that petal size was the only floral trait that may have diverged more than expected due to drift alone, but inflorescence height, flowering time, and rosette formation have greatly diverged between the native and nonnative populations. Our results suggest the loss of a rosette and the evolution of early flowering time may have been the key adaptations enabling wild radish to become a major agricultural weed. Floral adaptation to different pollinators does not seem to have been as necessary for the success of wild radish in new environments.     

Adaptive divergence for a fitness-related trait among invasive Ambrosia artemisiifolia populations in France

The impact of natural selection on the adaptive divergence of invasive populations can be assessed by testing the null hypothesis that the extent of quantitative genetic differentiation (Q(ST) ) would be similar to that of neutral molecular differentiation (F(ST) ). Using eight microsatellite loci and a common garden approach, we compared Q(ST) and F(ST) among ten populations of an invasive species Ambrosia artemisiifolia (common ragweed) in France. In a common garden study with varying water and nutrient levels, we measured Q(ST) for five traits (height, total biomass, reproductive allocation, above- to belowground biomass ratio, and days to flowering). Although low F(ST) indicated weak genetic structure and strong gene flow among populations, we found significant diversifying selection (Q(ST) > F(ST) ) for reproductive allocation that may be closely related to fitness. It suggests that abiotic conditions may have exerted selection pressure on A. artemisiifolia populations to differentiate adaptively, such that populations at higher altitude or latitude evolved greater reproductive allocation. As previous studies indicate multiple introductions from various source populations of A. artemisiifolia in North America, our results suggest that the admixture of introduced populations may have increased genetic diversity and additive genetic variance, and in turn, promoted the rapid evolution and adaptation of this invasive species.     

Molecular and quantitative genetic differentiation across Europe in yellow dung flies

Relating geographic variation in quantitative traits to underlying population structure is crucial for understanding processes driving population differentiation, isolation and ultimately speciation. Our study represents a comprehensive population genetic survey of the yellow dung fly Scathophaga stercoraria, an important model organism for evolutionary and ecological studies, over a broad geographic scale across Europe (10 populations from the Swiss Alps to Iceland). We simultaneously assessed differentiation in five quantitative traits (body size, development time, growth rate, proportion of diapausing individuals and duration of diapause), to compare differentiation in neutral marker loci (F(ST)) to that of quantitative traits (Q(ST)). Despite long distances and uninhabitable areas between sampled populations, population structuring was very low but significant (F(ST) = 0.007, 13 microsatellite markers; F(ST) = 0.012, three allozyme markers; F(ST) = 0.007, markers combined). However, only two populations (Iceland and Sweden) showed significant allelic differentiation to all other populations. We estimated high levels of gene flow [effective number of migrants (Nm) = 6.2], there was no isolation by distance, and no indication of past genetic bottlenecks (i.e. founder events) and associated loss of genetic diversity in any northern or island population. In contrast to the low population structure, quantitative traits were strongly genetically differentiated among populations, following latitudinal clines, suggesting that selection is responsible for life history differentiation in yellow dung flies across Europe.     

Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria)

Studies examining the effects of anthropogenic habitat fragmentation on both neutral and adaptive genetic variability are still scarce. We compared tadpole fitness-related traits (viz. survival probability and body size) among populations of the common frog (Rana temporaria) from fragmented (F) and continuous (C) habitats that differed significantly in population sizes (C > F) and genetic diversity (C > F) in neutral genetic markers. Using data from common garden experiments, we found a significant positive relationship between the mean values of the fitness related traits and the amount of microsatellite variation in a given population. While genetic differentiation in neutral marker loci (F(ST)) tended to be more pronounced in the fragmented than in the continuous habitat, genetic differentiation in quantitative traits (Q(ST)) exceeded that in neutral marker traits in the continuous habitat (i.e. Q(ST) > F(ST)), but not in the fragmented habitat (i.e. Q(ST) approximately F(ST)). These results suggest that the impact of random genetic drift relative to natural selection was higher in the fragmented landscape where populations were small, and had lower genetic diversity and fitness as compared to populations in the more continuous landscape. The findings highlight the potential importance of habitat fragmentation in impairing future adaptive potential of natural populations.     

Ecological genetics and seed transfer guidelines for Pinus albicaulis (Pinaceae)

Whitebark pine (Pinus albicaulis Engelm.) has greatly declined throughout its range as a result of introduced disease, fire suppression, and other factors, and climate change is predicted to accelerate this decline. Restoration is needed; however, no information regarding the degree of local adaptation is available to guide these efforts. A seedling common-garden experiment was employed to assess genetic diversity and geographic differentiation (Q(ST)) of whitebark pine for traits involved in growth and adaptation to cold and to determine climatic variables revealing local adaptation. Seedlings from 48 populations were grown for two years and measured for height increment, biomass, root to shoot ratio, date of needle flush, fall and spring cold injury, and survival. Significant variation was observed among populations for most traits. The Q(ST) was low (0.07-0.14) for growth traits and moderate (0.36-0.47) for cold adaptation related traits, but varied by region. Cold adaptation traits were strongly correlated with mean temperature of the coldest month of population origins, while growth traits were generally correlated with growing season length. We recommend that seed transfer for restoration favor seed movement from milder to colder climates to a maximum of 1.9°C in mean annual temperature in the northern portion of the species range, and 1.0°C in the U. S. Rocky Mountains to avoid maladaptation to current conditions yet facilitate adaptation to future climates.     

Genetic isolation of fragmented populations is exacerbated by drift and selection

Reduced genetic variation at marker loci in small populations has been well documented, whereas the relationship between quantitative genetic variation and population size has attracted little empirical investigation. Here we demonstrate that both neutral and quantitative genetic variation are reduced in small populations of a fragmented plant metapopulation, and that both drift and selective change are enhanced in small populations. Measures of neutral genetic differentiation (F(ST)) and quantitative genetic differentiation (Q(ST)) in two traits were higher among small demes, and Q(ST) between small populations exceeded that expected from drift alone. This suggests that fragmented populations experience both enhanced genetic drift and divergent selection on phenotypic traits, and that drift affects variation in both neutral markers and quantitative traits. These results highlight the need to integrate natural selection into conservation genetic theory, and suggests that small populations may represent reservoirs of genetic variation adaptive within a wide range of environments.     

Variation for neutral markers is correlated with variation for quantitative traits in the plant pathogenic fungus Mycosphaerella graminicola

We compared genetic variation and population differentiation at RFLP marker loci with seven quantitative characters including fungicide resistance, temperature sensitivity, pycnidial size, pycnidial density, colony size, percentage of leaves covered by pycnidia (PLACP) and percentage of leaves covered by lesions (PLACL) in Mycosphaerella graminicola populations sampled from four regions. Wide variation in population differentiation was found across the quantitative traits assayed. Fungicide resistance, temperature sensitivity, and PLACP displayed a significantly higher Q(ST) than G(ST), consistent with selection for local adaptation, while pycnidial size, pycnidial density and colony size displayed a lower or significantly lower Q(ST) than G(ST), consistent with constraining selection. There was not a statistical difference between Q(ST) and G(ST) in PLACL. We also found a positive and significant correlation between genetic variation in molecular marker loci and quantitative traits at the multitrait scale, suggesting that estimates of overall genetic variation for quantitative traits in M. graminicola could be derived from analysis of the molecular genetic markers.     

Comparison of population genetic structures of common wild rice (Oryza rufipogon Griff.), as revealed by analyses of quantitative traits, allozymes, and RFLPs

We investigated genetic diversity among and within natural populations of Asian common wild rice, Oryza rufipogon, from three different classes of data: quantitative traits, allozymes, and restriction fragment length polymorphisms (RFLPs). The seven populations examined showed polymorphism to varying degrees. The amount of intrapopulation variability appeared to be influenced not only by breeding system but also by the evolutionary history of each population. Interpopulation differentiation was clear, but different classes of data elucidated different patterns. Quantitative traits revealed ecotype differentiation into perennial and annual types of population, whereas allozyme and RFLP analyses revealed geographical differentiation among populations. These results suggest that the diversity patterns shown by quantitative trait analysis reflect mainly the occurrence of adaptive differentiation in response to habitat conditions and that those shown by allozyme and RFLP analyses reflect mainly the effect of isolation by distance. Population differentiation parameters (F(ST)) were highly variable among loci in allozymes as well as in RFLPs.     

Experimental demonstration of a causal relationship between heterogeneity of selection and genetic differentiation in quantitative traits

Comparisons of estimates of genetic differentiation at molecular markers (F(ST)) and at quantitative traits (Q(ST)) are a means of inferring the level and heterogeneity of selection in natural populations. However, such comparisons are questionable because they require that the influence of drift and selection on Q(ST) be detectable over possible background influences of environmental or nonadditive genetic effects on Q(ST)-values. Here we test this using an experimental evolution approach in metapopulations of Arabidopsis thaliana experiencing different levels of drift and selection heterogeneity. We estimated the intensity and heterogeneity of selection on morphological and phenological traits via selection differentials. We demonstrate that Q(ST)-values increased with increasing selection heterogeneity when genetic drift was limited. The effect of selection on Q(ST) was thus detectable despite significant genotype-by-environment interactions that most probably biased the estimates of genetic differentiation. Although they cannot be used as a direct validation of the conclusions of prior studies, our results strongly support both the relevance of Q(ST) as an estimator of genetic differentiation and the role of local selection in shaping the genetic differentiation of natural populations.     

Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis

Comparative studies of quantitative genetic and neutral marker differentiation have provided means for assessing the relative roles of natural selection and random genetic drift in explaining among-population divergence. This information can be useful for our fundamental understanding of population differentiation, as well as for identifying management units in conservation biology. Here, we provide comprehensive review and meta-analysis of the empirical studies that have compared quantitative genetic (Q(ST)) and neutral marker (F(ST)) differentiation among natural populations. Our analyses confirm the conclusion from previous reviews - based on ca. 100% more data - that the Q(ST) values are on average higher than F(ST) values [mean difference 0.12 (SD 0.27)] suggesting a predominant role for natural selection as a cause of differentiation in quantitative traits. However, although the influence of trait (life history, morphological and behavioural) and marker type (e.g. microsatellites and allozymes) on the variance of the difference between Q(ST) and F(ST) is small, there is much heterogeneity in the data attributable to variation between specific studies and traits. The latter is understandable as there is no reason to expect that natural selection would be acting in similar fashion on all populations and traits (except for fitness itself). We also found evidence to suggest that Q(ST) and F(ST) values across studies are positively correlated, but the significance of this finding remains unclear. We discuss these results in the context of utility of the Q(ST)-F(ST) comparisons as a tool for inferring natural selection, as well as associated methodological and interpretational problems involved with individual and meta-analytic studies.     

A Comparison of Isozyme and Quantitative Genetic Variation in Pinus Contorta Ssp. Latifolia by F(st)

We employed F-statistics to analyze quantitative and isozyme variation among five populations of Pinus contorta ssp. latifolia, a wind-pollinated outcrossing conifer with wide and continuous distribution in west North America. Estimates of population differentiation (F(ST)) for six quantitative traits were compared with the overall estimate of the differentiation (F*(ST)) from 19 isozymes that tested neutral to examine whether similar evolutionary processes were involved in morphological and isozyme differentiation. While the F(ST) estimates for specific gravity, stem diameter, stem height and branch length were significantly greater than the F*(ST) estimate, as judged from the 95% confidence intervals by bootstrapping, the F(ST) estimates for branch angle and branch diameter were indistinguishable from the F*(ST) estimate. Differentiation in stem height and stem diameter might reflect the inherent adaptation of the populations for rapid growth to escape suppression by neighboring plants during establishment and to regional differences in photoperiod, precipitation and temperature. In contrast, divergences in wood specific gravity and branch length might be correlated responses to population differentiation in stem growth. Possible bias in the estimation of F(ST) due to Hardy-Weinberg disequilibrium (F(IS) & 0), linkage disequilibrium, maternal effects and nonadditive genetic effects was discussed with special reference to P. contorta ssp. latifolia.     

The genetic differentiation at quantitative trait loci under local adaptation

Most adaptive traits are controlled by large number of genes that may all together be the targets of selection. Adaptation may thus involve multiple but not necessarily substantial allele frequency changes. This has important consequences for the detection of selected loci and implies that a quantitative genetics framework may be more appropriate than the classical 'selective sweep' paradigm. Preferred methods to detect loci involved in local adaptation are based on the detection of 'outlier' values of the allelic differentiation F(ST) . A quantitative genetics framework is adopted here to review theoretical expectations for how allelic differentiation at quantitative trait loci (F(STQ) ) relates to (i), neutral genetic differentiation (F(ST) ) and (ii), phenotypic differentiation (Q(ST) ). We identify cases where results of outlier-based methods are likely to be poor and where differentiation at selected loci conveys little information regarding local adaptation. A first case is when neutral differentiation is high, so that local adaptation does not necessitate increased differentiation. A second case is when local adaptation is reached via an increased covariance of allelic effects rather than via allele frequency changes, which is more likely under high gene flow when the number of loci is high and selection is recent. The comparison of theoretical predictions with observed data from the literature suggests that polygenic local adaptation involving only faint allele frequency changes are very likely in some species such as forest trees and for climate-related traits. Recent methodological improvements that may alleviate the weakness of F(ST) -based detection methods are presented.     

Genetic variation at allozyme and RAPD markers in Pinus longaeva (Pinaceae) of the White Mountains, California

We compared genetic diversity estimated from allozymes and from random amplified polymorphic DNA (RAPDs) in a sample of 210 Great Basin bristlecone pines (Pinus longaeva Bailey) from three groves in the White Mountains, California, USA. The White Mountains are the most westerly extension of bristlecone pine and home to the oldest known living trees. We assayed two forks of each tree to determine whether they originated from multiple seed caches of the Clark's nutcracker. Despite the limited and fragmented distribution of bristlecone pine, its level of genetic diversity was comparable to that of other pines, but lower than that reported for eastern populations of Great Basin bristlecone pine. Twenty-six of 36 allozymes were polymorphic (p(95) = 38.9%; p = 63.0%), with observed heterozygosity (H(o)) of 0.122 and expected heterozygosity (H(e)) of 0.134. The proportion of the total variation among populations (G(ST)) was only 0.011. The high proportion of trees with multiple stems was not due to germination in seed caches; only six of 210 forked trees had multiple allozyme genotypes. Of the 42 RAPD loci scored, 27 were monomorphic. Genetic diversity for RAPDs was nearly the same as that for allozymes (p(95) = 34.1%, H(e) = 0.130). However, the estimates of diversity and differentiation were much higher (H(e) = 0.321, G(ST) = 0.039) after excluding monomorphic loci.     

The effects of dominance, regular inbreeding and sampling design on Q(ST), an estimator of population differentiation for quantitative traits

To test whether quantitative traits are under directional or homogenizing selection, it is common practice to compare population differentiation estimates at molecular markers (F(ST)) and quantitative traits (Q(ST)). If the trait is neutral and its determinism is additive, then theory predicts that Q(ST) = F(ST), while Q(ST) > F(ST) is predicted under directional selection for different local optima, and Q(ST) < F(ST) is predicted under homogenizing selection. However, nonadditive effects can alter these predictions. Here, we investigate the influence of dominance on the relation between Q(ST) and F(ST) for neutral traits. Using analytical results and computer simulations, we show that dominance generally deflates Q(ST) relative to F(ST). Under inbreeding, the effect of dominance vanishes, and we show that for selfing species, a better estimate of Q(ST) is obtained from selfed families than from half-sib families. We also compare several sampling designs and find that it is always best to sample many populations (>20) with few families (five) rather than few populations with many families. Provided that estimates of Q(ST) are derived from individuals originating from many populations, we conclude that the pattern Q(ST) > F(ST), and hence the inference of directional selection for different local optima, is robust to the effect of nonadditive gene actions.     

Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce

Patterns of variation in quantitative characters and genetic markers were compared among six regional populations of white spruce [Picea glauca (Moench) Voss]. Although some phenotypic characters were correlated with latitude (r = 0.791), longitude (r = -0.796) and precipitation during the growing season (r = 0.789), variability at genetic markers was not correlated with geographical or bioclimatic variables, and followed neutral expectations. Estimates of genetic diversity and population differentiation for 14 allozymes (translated regions of coding genes) were essentially indistinguishable from those observed for 11 expressed sequence tag polymorphisms (ESTPs) from untranslated regions of coding genes. Variation among populations for quantitative traits such as eighth year height (Q(ST) = 0.082), thirteenth year height (Q(ST) = 0.069), total wood density (Q(ST) = 0.102) and date of budset (Q(ST) = 0.246), was greater than for allozymes (G(ST) = 0.014) and ESTPs (G(ST) = 0.019). These trends suggest a strong adaptive response in quantitative traits, contrasting to allozymes and ESTPs where no selective response could be detected and where populations appeared to be essentially in a migration-drift equilibrium.     

Molecular and quantitative genetic divergence among populations of house mice with known evolutionary histories

Evolutionary biologists have long been interested in the processes influencing population differentiation, but separating the effects of neutral and adaptive evolution has been an obstacle for studies of population subdivision. A recently developed method allows tests of whether disruptive (ie, spatially variable) or stabilizing (ie, spatially uniform) selection is influencing phenotypic differentiation among subpopulations. This method, referred to as the F(ST) vs Q(ST) comparison, separates the total additive genetic variance into within- and among-population components and evaluates this level of differentiation against a neutral hypothesis. Thus, levels of neutral molecular (F(ST)) and quantitative genetic (Q(ST)) divergence are compared to evaluate the effects of selection and genetic drift on phenotypic differentiation. Although the utility of such comparisons appears great, its accuracy has not yet been evaluated in populations with known evolutionary histories. In this study, F(ST) vs Q(ST) comparisons were evaluated using laboratory populations of house mice with known evolutionary histories. In this model system, the F(ST) vs Q(ST) comparisons between the selection groups should reveal quantitative trait differentiation consistent with disruptive selection, while the F(ST) vs Q(ST) comparisons among lines within the selection groups should suggest quantitative trait differentiation in agreement with drift. We find that F(ST) vs Q(ST) comparisons generally produce the correct evolutionary inference at each level in the population hierarchy. Additionally, we demonstrate that when strong selection is applied between populations Q(ST) increases relative to Q(ST) among populations diverging by drift. Finally, we show that the statistical properties of Q(ST), a variance component ratio, need further investigation.     

Linkage and Association Mapping for Two Major Traits Used in the Maritime Pine Breeding Program: Height Growth and Stem Straightness

BackgroundIncreasing our understanding of the genetic architecture of complex traits, through analyses of genotype-phenotype associations and of the genes/polymorphisms accounting for trait variation, is crucial, to improve the integration of molecular markers into forest tree breeding. In this study, two full-sib families and one breeding population of maritime pine were used to identify quantitative trait loci (QTLs) for height growth and stem straightness, through linkage analysis (LA) and linkage disequilibrium (LD) mapping approaches.ResultsThe populations used for LA consisted of two unrelated three-generation full-sib families (n = 197 and n = 477). These populations were assessed for height growth or stem straightness and genotyped for 248 and 217 markers, respectively. The population used for LD mapping consisted of 661 founders of the first and second generations of the breeding program. This population was phenotyped for the same traits and genotyped for 2,498 single-nucleotide polymorphism (SNP) markers corresponding to 1,652 gene loci. The gene-based reference genetic map of maritime pine was used to localize and compare the QTLs detected by the two approaches, for both traits. LA identified three QTLs for stem straightness and two QTLs for height growth. The LD study yielded seven significant associations (P ≤ 0.001): four for stem straightness and three for height growth. No colocalisation was found between QTLs identified by LA and SNPs detected by LD mapping for the same trait.ConclusionsThis study provides the first comparison of LA and LD mapping approaches in maritime pine, highlighting the complementary nature of these two approaches for deciphering the genetic architecture of two mandatory traits of the breeding program.     

Phenotypic and allozyme variation in Mediterranean and desert populations of wild barley,Hordeum spontaneum Koch

Populations of wild barley, Hordeum spontaneum Koch, were collected in two distinct climatic regions, desert and Mediterranean. Plants from five desert and five Mediterranean populations were compared and contrasted for extent and structure of phenotypic variation. These same 10 and one other population from each region were analyzed for allozyme variation. In a field trial of phenotypic diversity, two phenological and 14 morphological traits were examined. Study of allozyme variation was performed using eight enzyme systems encoding for 13 loci. Plants from the desert and Mediterranean regions were significantly different in seven of 16 phenotypic traits, exhibited a high (30%) interregional component of phenotypic variation, and showed a high degree of segregation on a principal component scattergram indicating ecotypic differentiation. Mediterranean populations were twice as variable as desert populations in reproductive growth parameters (stem and spike length) and grain filling (spikelet weight), but half as variable for onset of reproduction. The extent and structure of phenotypic and allozyme variation did not match. The Mediterranean and desert populations did not differ in amount of allozyme variation as estimated by mean number of alleles per locus, effective number of alleles, polymorphism, and gene diversity (n(a), n(e), P, and H(e)), did not segregate on the basis of population genetic distances, and exhibited a low proportion of interregion allozyme diversity (2%). No effect of selection on allozyme distribution was detected. Our results suggest that the adaptation of plants originating from desert and Mediterranean environments is reflected in phenotypic but not in allozyme variation.     

Maternal genetic effects on adaptive divergence between anadromous and resident brook charr during early life history

The importance of directional selection relative to neutral evolution may be determined by comparing quantitative genetic variation in phenotype (Q(ST)) to variation at neutral molecular markers (F(ST)). Quantitative divergence between salmonid life history types is often considerable, but ontogenetic changes in the significance of major sources of genetic variance during post-hatch development suggest that selective differentiation varies by developmental stage. In this study, we tested the hypothesis that maternal genetic differentiation between anadromous and resident brook charr (Salvelinus fontinalis Mitchill) populations for early quantitative traits (embryonic size/growth, survival, egg number and developmental time) would be greater than neutral genetic differentiation, but that the maternal genetic basis for differentiation would be higher for pre-resorption traits than post-resorption traits. Quantitative genetic divergence between anadromous (seawater migratory) and resident Laval River (Québec) brook charr based on maternal genetic variance was high (Q(ST) > 0.4) for embryonic length, yolk sac volume, embryonic growth rate and time to first response to feeding relative to neutral genetic differentiation [F(ST) = 0.153 (0.071-0.214)], with anadromous females having positive genetic coefficients for all of the above characters. However, Q(ST) was essentially zero for all traits post-resorption of the yolk sac. Our results indicate that the observed divergence between resident and anadromous brook charr has been driven by directional selection, and may therefore be adaptive. Moreover, they provide among the first evidence that the relative importance of selective differentiation may be highly context-specific, and varies by genetic contributions to phenotype by parental sex at specific points in offspring ontogeny. This in turn suggests that interpretations of Q(ST)-F(ST) comparisons may be improved by considering the structure of quantitative genetic architecture by age category and the sex of the parent used in estimation.