Effects of genetic drift on variance components under a general model of epistasis

We analyze the changes in the mean and variance components of a quantitative trait caused by changes in allele frequencies, concentrating on the effects of genetic drift. We use a general representation of epistasis and dominance that allows an arbitrary relation between genotype and phenotype for any number of diallelic loci. We assume initial and final Hardy-Weinberg and linkage equilibrium in our analyses of drift-induced changes. Random drift generates transient linkage disequilibria that cause correlations between allele frequency fluctuations at different loci. However, we show that these have negligible effects, at least for interactions among small numbers of loci. Our analyses are based on diffusion approximations that summarize the effects of drift in terms of F, the inbreeding coefficient, interpreted as the expected proportional decrease in heterozygosity at each locus. For haploids, the variance of the trait mean after a population bottleneck is var(delta(z)) = sigma(n)k=1 FkV(A(k)), where n is the number of loci contributing to the trait variance, V(A(1)) = V(A) is the additive genetic variance, and V(A(k)) is the kth-order additive epistatic variance. The expected additive genetic variance after the bottleneck, denoted (V*(A)), is closely related to var(delta(z)); (V*(A)) = (1 - F) sigma(n)k=1 kFk-1V(A(k)). Thus, epistasis inflates the expected additive variance above V(A)(1 - F), the expectation under additivity. For haploids (and diploids without dominance), the expected value of every variance component is inflated by the existence of higher order interactions (e.g., third-order epistasis inflates (V*(AA. This is not true in general with diploidy, because dominance alone can reduce (V*(A)) below V(A)(1 - F) (e.g., when dominant alleles are rare). Without dominance, diploidy produces simple expressions: var(delta(z)) = sigma(n)k=1 (2F)kV(A(k)) and (V(A)) = (1 - F) sigma(n)k=1 k(2F)k-1V(A(k)). With dominance (and even without epistasis), var(delta(z)) and (V*(A)) no longer depend solely on the variance components in the base population. For small F, the expected additive variance simplifies to (V*(A)) approximately equal to (1 - F)V(A) + 4FV(AA) + 2FV(D) + 2FC(AD), where C(AD) is a sum of two terms describing covariances between additive effects and dominance and additive X dominance interactions. Whether population bottlenecks lead to expected increases in additive variance depends primarily on the ratio of nonadditive to additive genetic variance in the base population, but dominance precludes simple predictions based solely on variance components. We illustrate these results using a model in which genotypic values are drawn at random, allowing extreme and erratic epistatic interactions. Although our analyses clarify the conditions under which drift is expected to increase V(A), we question the evolutionary importance of such increases.     

Change in Genetic Variance under Selection in a Self-Fertilizing Population

In this study we show how the genetic variance of a quantitative trait changes in a self-fertilizing population under repeated cycles of truncation selection, with the analysis based on the infinitesimal model in which it is assumed that the trait is determined by an infinite number of unlinked loci without epistasis. The genetic variance is reduced not as a consequence of the genotypic frequency change but due to the build-up of linkage disequilibrium under truncation selection in this model. We assume that the order of the genotypic contribution from each locus is n(-1/2), where n is the number of loci involved, and investigate the change in linkage disequilibrium resulting from selection and self-fertilization using genotypic frequency dynamics in order to analyze the change in the genetic variance. Our analysis gives recurrence relations of genetic variance among the succeeding generations for the three cases of gene action, i.e., purely additive action, pure dominance without additive effect and the presence of both additive effect and dominance, respectively. Numerical examples are also given as a check on the recurrence formulas.     

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load

Sexual selection on males is predicted to increase population fitness, and delay population extinction, when mating success negatively covaries with genetic load across individuals. However, such benefits of sexual selection could be counteracted by simultaneous increases in genome-wide drift resulting from reduced effective population size caused by increased variance in fitness. Resulting fixation of deleterious mutations could be greatest in small populations, and when environmental variation in mating traits partially decouples sexual selection from underlying genetic variation. The net consequences of sexual selection for genetic load and population persistence are therefore likely to be context dependent, but such variation has not been examined. We use a genetically explicit individual-based model to show that weak sexual selection can increase population persistence time compared to random mating. However, for stronger sexual selection such positive effects can be overturned by the detrimental effects of increased genome-wide drift. Furthermore, the relative strengths of mutation-purging and drift critically depend on the environmental variance in the male mating trait. Specifically, increasing environmental variance caused stronger sexual selection to elevate deleterious mutation fixation rate and mean selection coefficient, driving rapid accumulation of drift load and decreasing population persistence times. These results highlight an intricate balance between conflicting positive and negative consequences of sexual selection on genetic load, even in the absence of sexually antagonistic selection. They imply that environmental variances in key mating traits, and intrinsic genetic drift, should be properly factored into future theoretical and empirical studies of the evolution of population fitness under sexual selection.     

Non-additive genetic variation in growth,carcass and fertility traits of beef cattle

Background

A better understanding of non-additive variance could lead to increased knowledge on the genetic control and physiology of quantitative traits, and to improved prediction of the genetic value and phenotype of individuals. Genome-wide panels of single nucleotide polymorphisms (SNPs) have been mainly used to map additive effects for quantitative traits, but they can also be used to investigate non-additive effects. We estimated dominance and epistatic effects of SNPs on various traits in beef cattle and the variance explained by dominance, and quantified the increase in accuracy of phenotype prediction by including dominance deviations in its estimation.

Methods

Genotype data (729 068 real or imputed SNPs) and phenotypes on up to 16 traits of 10 191 individuals from Bos taurus, Bos indicus and composite breeds were used. A genome-wide association study was performed by fitting the additive and dominance effects of single SNPs. The dominance variance was estimated by fitting a dominance relationship matrix constructed from the 729 068 SNPs. The accuracy of predicted phenotypic values was evaluated by best linear unbiased prediction using the additive and dominance relationship matrices. Epistatic interactions (additive × additive) were tested between each of the 28 SNPs that are known to have additive effects on multiple traits, and each of the other remaining 729 067 SNPs.

Results

The number of significant dominance effects was greater than expected by chance and most of them were in the direction that is presumed to increase fitness and in the opposite direction to inbreeding depression. Estimates of dominance variance explained by SNPs varied widely between traits, but had large standard errors. The median dominance variance across the 16 traits was equal to 5% of the phenotypic variance. Including a dominance deviation in the prediction did not significantly increase its accuracy for any of the phenotypes. The number of additive × additive epistatic effects that were statistically significant was greater than expected by chance.

Conclusions

Significant dominance and epistatic effects occur for growth, carcass and fertility traits in beef cattle but they are difficult to estimate precisely and including them in phenotype prediction does not increase its accuracy.     

Estimation of additive, dominance and epistatic variance components using finite locus models implemented with a single-site Gibbs and a descent graph sampler

In a previous contribution, we implemented a finite locus model (FLM) for estimating additive and dominance genetic variances via a Bayesian method and a single-site Gibbs sampler. We observed a dependency of dominance variance estimates on locus number in the analysis FLM. Here, we extended the FLM to include two-locus epistasis, and implemented the analysis with two genotype samplers (Gibbs and descent graph) and three different priors for genetic effects (uniform and variable across loci, uniform and constant across loci, and normal). Phenotypic data were simulated for two pedigrees with 6300 and 12,300 individuals in closed populations, using several different, non-additive genetic models. Replications of these data were analysed with FLMs differing in the number of loci. Simulation results indicate that the dependency of non-additive genetic variance estimates on locus number persisted in all implementation strategies we investigated. However, this dependency was considerably diminished with normal priors for genetic effects as compared with uniform priors (constant or variable across loci). Descent graph sampling of genotypes modestly improved variance components estimation compared with Gibbs sampling. Moreover, a larger pedigree produced considerably better variance components estimation, suggesting this dependency might originate from data insufficiency. As the FLM represents an appealing alternative to the infinitesimal model for genetic parameter estimation and for inclusion of polygenic background variation in QTL mapping analyses, further improvements are warranted and might be achieved via improvement of the sampler or treatment of the number of loci as an unknown.     

Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila

According to neutral quantitative genetic theory, population bottlenecks are expected to decrease standing levels of additive genetic variance of quantitative traits. However, some empirical and theoretical results suggest that, if nonadditive genetic effects influence the trait, bottlenecks may actually increase additive genetic variance. This has been an important issue in conservation genetics where it has been suggested that small population size might actually experience an increase rather than a decrease in the rate of adaptation. Here we test if bottlenecks can break a selection limit for desiccation resistance in the rain forest-restricted fly Drosophila bunnanda. After one generation of single-pair mating, additive genetic variance for desiccation resistance increased to a significant level, on average higher than for the control lines. Line crosses revealed that both dominance and epistatic effects were responsible for the divergence in desiccation resistance between the original control and a bottlenecked line exhibiting increased additive genetic variance for desiccation resistance. However, when bottlenecked lines were selected for increased desiccation resistance, there was only a small shift in resistance, much less than predicted by the released additive genetic variance. The small selection response in the bottlenecked lines was no greater than that observed in the control lines. Thus bottlenecks might produce a statistically detectable change in additive genetic variance but this change has no impact on the response to selection.     

The effect of genetic drift on the variance/covariance components generated by multilocus additive x additive epistatic systems

The effect of population bottlenecks on the components of the genetic variance/covariance generated by n neutral independent additive x additive loci has been studied theoretically. In its simplest version, this situation can be modelled by specifying the allele frequencies and homozygous effects at each locus, and an additional factor measuring the strength of the n-th order epistatic interaction. The variance/covariance components in an infinitely large panmictic population (ancestral components) were compared with their expected values at equilibrium over replicates randomly derived from the base population, after t bottlenecks of size N (derived components). Formulae were obtained giving the derived components (and the between-line variance) as functions of the ancestral ones (alternatively, in terms of allele frequencies and effects) and the corresponding inbreeding coefficient F(t). The n-th order derived component of the genetic variance/covariance is continuously eroded by inbreeding, but the remaining components may increase initially until a critical F(t) value is attained, which is inversely related to the order of the pertinent component, and subsequently decline to zero. These changes can be assigned to the between-line variances/covariances of gene substitution and epistatic effects induced by drift. Numerical examples indicate that: (1) the derived additive variance/covariance component will generally exceed its ancestral value unless epistasis is weak; (2) the derived epistatic variance/covariance components will generally exceed their ancestral values unless allele frequencies are extreme; (3) for systems showing equal ancestral additive and total non-additive variance/covariance components, those including a smaller number of epistatic loci may generate a larger excess in additive variance/covariance after bottlenecks than others involving a larger number of loci, provided that F(t) is low. Our results indicate that it is unlikely that the rate of evolution may be significantly accelerated after population bottlenecks, in spite of occasional increments of the derived additive variance over its ancestral value.     

Mate choice for non-additive genetic benefits: a resolution to the lek paradox

In promiscuous mating systems, females often show a consistent preference to mate with one or a few males, presumably to acquire heritable genetic benefits for their offspring. However, strong directional selection should deplete additive genetic variation in fitness and consequently any benefit to expressing the preference by females (referred to as the lek paradox). Here, we provide a novel resolution that examines non-additive genetic benefits, such as overdominance or inbreeding, as a source of genetic variation. Focusing on the inbreeding coefficient f and overdominance effects, we use dynamic models to show that (1) f can be inherited from sire to offspring, (2) populations with females that express a mating preferences for outbred males (low f) maintain higher genetic variation than populations with females that mate randomly, and (3) preference alleles for outbred males can invade populations even when the alleles are associated with a fecundity cost. We show that non-additive genetic variation due to overdominance can be converted to additive genetic variation and becomes “heritable” when the frequencies of alternative homozygous genotypes at fitness loci deviate from equality. Unlike previous models that assume an infinite population size, we now show that genetic drift in finite populations can lead to the necessary deviations in the frequencies of homozygous genotypes. We also show that the “heritability of f,” and hence the benefit to a mating preference for non-additive genetic benefits, is highest in small populations and populations in which a smaller number of loci contribute to fitness via overdominance. Our model contributes to the solution of the lek paradox.     

Combined genetic analysis of partial blast resistance in an upland rice population and recurrent selection for line and hybrid values

The CNA-IRAT 5 upland rice population has been improved for 4 years by recurrent selection for blast resistance in Brazil. In order to predict the efficiency of recurrent selection in different test systems and to compare the relative advantage of hybrids versus pure line breeding, a combined genetic analysis of partial blast resistance in the CNA-IRAT 5 population was undertaken. A three-level hierarchical design in inbreeding and a factorial design were derived from the base population. Partial blast resistance of lines and hybrids was evaluated in the greenhouse and in the field by inoculation with one virulent blast isolate. The means and genetic variances of the hybrids and lines were estimated. Genetic advance by recurrent selection was predicted from estimates of variance components. The inheritance of partial blast resistance was mainly additive but non-additive effects were detected at both levels of means and variances. Mean heterosis ranged from 4%–8% for lesion size and lesion density to 10–12% for leaf and panicle resistance. High dominance or homozygous dominance variances relative to additive variance and negative covariance between additive and homozygous dominance effects were estimated. A low frequency of favourable alleles for partial resistance would explain the observed organisation of genetic variability in the base population. Recurrent selection will efficiently improve partial blast resistance of the CNA-IRAT 5 population. Genetic advance for line or hybrid values was expected to be higher testing doubled haploid lines than S1 lines, or than general combining ability. Two components of partial resistance assessed in the greenhouse, lesion size and lesion density, could be used as indirect selection criteria to improve field resistance. On the whole, hybrid breeding for partial blast resistance appeared to be slightly more advantageous than pure line breeding.     

Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana

The effects of a single population bottleneck of differing severity on heritability and additive genetic variance was investigated experimentally using a butterfly. An outbred laboratory stock was used to found replicate lines with one pair, three pairs and 10 pairs of adults, as well as control lines with approximately 75 effective pairs. Heritability and additive genetic variance of eight wing pattern characters and wing size were estimated using parent-offspring covariances in the base population and in all daughter lines. Individual morphological characters and principal components of the nine characters showed a consistent pattern of treatment effects in which average heritability and additive genetic variance was lower in one pair and three pair lines than in 10 pair and control lines. Observed losses in heritability and additive genetic variance were significantly greater than predicted by the neutral additive model when calculated with coefficients of inbreeding estimated from demographic parameters alone. However, use of molecular markers revealed substantially more inbreeding, generated by increased variance in family size and background selection. Conservative interpretation of a statistical analysis incorporating this previously undetected inbreeding led to the conclusion that the response to inbreeding of the morphological traits studied showed no significant departure from the neutral additive model. This result is consistent with the evidence for minimal directional dominance for these traits. In contrast, egg hatching rate in the same experimental lines showed strong inbreeding depression, increased phenotypic variance and rapid response to selection, highly indicative of an increase in additive genetic variance due to dominance variance conversion.     

Estimates of genetic variance in an F2 maize population

Maize (Zea mays L.) breeders have used several genetic-statistical models to study the inheritance of quantitative traits. These models provide information on the importance of additive, dominance, and epistatic genetic variance for a quantitative trait. Estimates of genetic variances are useful in understanding heterosis and determining the response to selection. The objectives of this study were to estimate additive and dominance genetic variances and the average level of dominance for an F2 population derived from the B73 x Mo17 hybrid and use weighted least squares to determine the importance of digenic epistatic variances relative to additive and dominance variances. Genetic variances were estimated using Design III and weighted least squares analyses. Both analyses determined that dominance variance was more important than additive variance for grain yield. For other traits, additive genetic variance was more important than dominance variance. The average level of dominance suggests either overdominant gene effects were present for grain yield or pseudo-overdominance because of linkage disequilibrium in the F2 population. Epistatic variances generally were not significantly different from zero and therefore were relatively less important than additive and dominance variances. For several traits estimates of additive by additive epistatic variance decreased estimates of additive genetic variance, but generally the decrease in additive genetic variance was not significant.     

Prediction of effects of genetic drift on variance components under a general model of epistasis

For a model of diallelic loci with arbitrary epistasis, Barton and Turelli [2004. Effects of genetic drift on variance components under a general model of epistasis. Evolution 58, 2111-2132] gave results for variances among and within replicate lines obtained by inbreeding without selection. Here, we discuss the relation between their population genetic methods and classical quantitative genetic arguments. In particular, we consider the case of no dominance using classical identity by descent arguments, which generalizes their results from two alleles to multiple alleles. To clarify the connections between the alternative methods, we obtain the same results using an intermediate method, which explicitly identifies the statistical effects of sets of loci. We also discuss the effects of population bottlenecks on covariances among relatives.     

Non-additive genetic effects for fertility traits in Canadian Holstein cattle (Open Access publication )

The effects of additive, dominance, additive by dominance, additive by additive and dominance by dominance genetic effects on age at first service, non-return rates and interval from calving to first service were estimated. Practical considerations of computing additive and dominance relationships using the genomic relationship matrix are discussed. The final strategy utilized several groups of 1000 animals (heifers or cows) in which all animals had a non-zero dominance relationship with at least one other animal in the group. Direct inversion of relationship matrices was possible within the 1000 animal subsets. Estimates of variances were obtained using Bayesian methodology via Gibbs sampling. Estimated non-additive genetic variances were generally as large as or larger than the additive genetic variance in most cases, except for non-return rates and interval from calving to first service for cows. Non-additive genetic effects appear to be of sizeable magnitude for fertility traits and should be included in models intended for estimating additive genetic merit. However, computing additive and dominance relationships for all possible pairs of individuals is very time consuming in populations of more than 200 000 animals.     

Effect of mass selection on the within-family genetic variance in finite populations

Summary The adequacy of an expression for the withinfamily genetic variance under pure random drift in an additive infinitesimal model was tested via simulation in populations undergoing mass selection. Two hundred or one thousand unlinked loci with two alleles at initial frequencies of 1/2 were considered. The size of the population was 100 (50 males and 50 females). Full-sib matings were carried out for 15 generations with only one male and one female chosen as parents each generation, either randomly or on an individual phenotypic value. In the unselected population, results obtained from 200 replicates were in agreement with predictions. With mass selection, within-family genetic variance was overpredicted by theory from the 12th and 4th generations for the 1,000 and 200 loci cases, respectively. Taking into account the observed change in gene frequencies in the algorithm led to a much better agreement with observed values. Results for the distribution of gene frequencies and the withinlocus genetic covariance are presented. It is concluded that the expression for the within-family genetic variance derived for pure random drift holds well for mass selection within the limits of an additive infinitesimal model.     

The change in quantitative genetic variation with inbreeding

Inbreeding is known to reduce heterozygosity of neutral genetic markers, but its impact on quantitative genetic variation is debated. Theory predicts a linear decline in additive genetic variance (V(A)) with increasing inbreeding coefficient (F) when loci underlying the trait act additively, but a nonlinear hump-shaped relationship when dominance and epistasis are important. Predictions for heritability (h2) are similar, although the exact shape depends on the value of h2 in the absence of inbreeding. We located 22 published studies in which the level of genetic variation in experimentally inbred populations (measured by V(A) or h2) was compared with that in outbred control populations. For life-history traits, the data strongly supported a nonlinear change in genetic variation with increasing F. V(A) and h2 were, respectively, 244% and 50% higher at F = 0.4 than in outbred populations, and dominance plus epistatic variance together exceeded additive variance by a factor of four. For nonfitness traits the decline was linear and estimates of nonadditive variance were small. These results confirm that population bottlenecks frequently increase V(A) in some traits, and imply that life-history traits are underlain by substantial dominance or epistasis. However, the importance of drift-induced genetic variation in conservation or evolutionary biology is questionable, in part because inbreeding depression usually accompanies inbreeding.     

The reality and importance of founder speciation in evolution

A founder event occurs when a new population is established from a small number of individuals drawn from a large ancestral population. Mayr proposed that genetic drift in an isolated founder population could alter the selective forces in an epistatic system, an observation supported by recent studies. Carson argued that a period of relaxed selection could occur when a founder population is in an open ecological niche, allowing rapid population growth after the founder event. Selectable genetic variation can actually increase during this founder-flush phase due to recombination, enhanced survival of advantageous mutations, and the conversion of non-additive genetic variance into additive variance in an epistatic system, another empirically confirmed prediction. Templeton combined the theories of Mayr and Carson with population genetic models to predict the conditions under which founder events can contribute to speciation, and these predictions are strongly confirmed by the empirical literature. Much of the criticism of founder speciation is based upon equating founder speciation to an adaptive peak shift opposed by selection. However, Mayr, Carson and Templeton all modeled a positive interaction of selection and drift, and Templeton showed that founder speciation is incompatible with peak-shift conditions. Although rare, founder speciation can have a disproportionate importance in adaptive innovation and radiation, and examples are given to show that "rare" does not mean "unimportant" in evolution. Founder speciation also interacts with other speciation mechanisms such that a speciation event is not a one-dimensional process due to either selection alone or drift alone.     

Data and theory point to mainly additive genetic variance for complex traits

The relative proportion of additive and non-additive variation for complex traits is important in evolutionary biology, medicine, and agriculture. We address a long-standing controversy and paradox about the contribution of non-additive genetic variation, namely that knowledge about biological pathways and gene networks imply that epistasis is important. Yet empirical data across a range of traits and species imply that most genetic variance is additive. We evaluate the evidence from empirical studies of genetic variance components and find that additive variance typically accounts for over half, and often close to 100%, of the total genetic variance. We present new theoretical results, based upon the distribution of allele frequencies under neutral and other population genetic models, that show why this is the case even if there are non-additive effects at the level of gene action. We conclude that interactions at the level of genes are not likely to generate much interaction at the level of variance.     

Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster

Fecundity is usually considered as a trait closely connected to fitness and is expected to exhibit substantial nonadditive genetic variation and inbreeding depression. However, two independent experiments, using populations of different geographical origin, indicate that early fecundity in Drosophila melanogaster behaves as a typical additive trait of low heritability. The first experiment involved artificial selection in inbred and non-inbred lines, all of them started from a common base population previously maintained in the laboratory for about 35 generations. The realized heritability estimate was 0.151 +/- 0.075 and the inbreeding depression was very small and nonsignificant (0.09 +/- 0.09% of the non-inbred mean per 1% increase in inbreeding coefficient). With inbreeding, the observed decrease in the within-line additive genetic variance and the corresponding increase of the between-line variance were very close to their expected values for pure additive gene action. This result is at odds with previous studies showing inbreeding depression and, therefore, directional dominance for the same trait and species. All experiments, however, used laboratory populations, and it is possible that the original genetic architecture of the trait in nature was subsequently altered by the joint action of random drift and adaptation to captivity. Thus, we carried out a second experiment, involving inbreeding without artificial selection in a population recently collected from the wild. In this case we obtained, again, a maximum-likelihood heritability estimate of 0.210 +/- 0.027 and very little nonsignificant inbreeding depression (0.06 +/- 0.12%). The results suggest that, for fitness-component traits, low levels of additive genetic variance are not necessarily associated with large inbreeding depression or high levels of nonadditive genetic variance.     

Estimating Additive and Non-Additive Genetic Variances and Predicting Genetic Merits Using Genome-Wide Dense Single Nucleotide Polymorphism Markers

Non-additive genetic variation is usually ignored when genome-wide markers are used to study the genetic architecture and genomic prediction of complex traits in human, wild life, model organisms or farm animals. However, non-additive genetic effects may have an important contribution to total genetic variation of complex traits. This study presented a genomic BLUP model including additive and non-additive genetic effects, in which additive and non-additive genetic relation matrices were constructed from information of genome-wide dense single nucleotide polymorphism (SNP) markers. In addition, this study for the first time proposed a method to construct dominance relationship matrix using SNP markers and demonstrated it in detail. The proposed model was implemented to investigate the amounts of additive genetic, dominance and epistatic variations, and assessed the accuracy and unbiasedness of genomic predictions for daily gain in pigs. In the analysis of daily gain, four linear models were used: 1) a simple additive genetic model (MA), 2) a model including both additive and additive by additive epistatic genetic effects (MAE), 3) a model including both additive and dominance genetic effects (MAD), and 4) a full model including all three genetic components (MAED). Estimates of narrow-sense heritability were 0.397, 0.373, 0.379 and 0.357 for models MA, MAE, MAD and MAED, respectively. Estimated dominance variance and additive by additive epistatic variance accounted for 5.6% and 9.5% of the total phenotypic variance, respectively. Based on model MAED, the estimate of broad-sense heritability was 0.506. Reliabilities of genomic predicted breeding values for the animals without performance records were 28.5%, 28.8%, 29.2% and 29.5% for models MA, MAE, MAD and MAED, respectively. In addition, models including non-additive genetic effects improved unbiasedness of genomic predictions.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.