A MULTIVARIATE ANALYSIS OF GENETIC VARIATION IN THE ADVERTISEMENT CALL OF THE GRAY TREEFROG,HYLA VERSICOLOR

Genetic variation in sexual displays is crucial for an evolutionary response to sexual selection, but can be eroded by strong selection. Identifying the magnitude and sources of additive genetic variance underlying sexually selected traits is thus an important issue in evolutionary biology. We conducted a quantitative genetics experiment with gray treefrogs (Hyla versicolor) to investigate genetic variances and covariances among features of the male advertisement call. Two energetically expensive traits showed significant genetic variation: call duration, expressed as number of pulses per call, and call rate, represented by its inverse, call period. These two properties also showed significant genetic covariance, consistent with an energetic constraint to call production. Combining the genetic variance–covariance matrix with previous estimates of directional sexual selection imposed by female preferences predicts a limited increase in call duration but no change in call rate despite significant selection on both traits. In addition to constraints imposed by the genetic covariance structure, an evolutionary response to sexual selection may also be limited by high energetic costs of long‐duration calls and by preferences that act most strongly against very short‐duration calls. Meanwhile, the persistence of these preferences could be explained by costs of mating with males with especially unattractive calls.     

SEX-SPECIFIC GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM: A SYSTEMATIC REVIEW OF CROSS-SEX GENETIC CORRELATIONS

The independent evolution of the sexes may often be constrained if male and female homologous traits share a similar genetic architecture. Thus, cross-sex genetic covariance is assumed to play a key role in the evolution of sexual dimorphism (SD) with consequent impacts on sexual selection, population dynamics, and speciation processes. We compiled cross-sex genetic correlations ( r _MF) estimates from 114 sources to assess the extent to which the evolution of SD is typically constrained and test several specific hypotheses. First, we tested if r _MF differed among trait types and especially between fitness components and other traits. We also tested the theoretical prediction of a negative relationship between r _MF and SD based on the expectation that increases in SD should be facilitated by sex-specific genetic variance. We show that r _MF is usually large and positive but that it is typically smaller for fitness components. This demonstrates that the evolution of SD is typically genetically constrained and that sex-specific selection coefficients may often be opposite in sign due to sub-optimal levels of SD. Most importantly, we confirm that sex-specific genetic variance is an important contributor to the evolution of SD by validating the prediction of a negative correlation between r _MF and SD.     

SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

SEXUAL CONFLICT AND THE MAINTENANCE OF MULTIVARIATE GENETIC VARIATION

Mate choice should erode additive genetic variation in sexual displays, yet these traits often harbor substantial genetic variation. Nevertheless, recent developments in quantitative genetics have suggested that multivariate genetic variation in the combinations of traits under selection may still be depleted. Accordingly, the erosion and maintenance of variation may only be detectable by studying whole suites of traits. One potential process favoring the maintenance of genetic variance in multiple trait combinations is the modification of sexual selection via sexually antagonistic interactions between males and females. Here we consider how interlocus sexual conflict can shape the genetic architecture of male sexual traits in the cricket, Teleogryllus commodus. In this species, the ability of each sex to manipulate insemination success significantly alters the selection acting on male courtship call properties. Using a quantitative genetic breeding design we estimated the additive genetic variation in these traits and then predicted the change in variation due to previously documented patterns of sexual selection. Our results indicate that female choice should indeed deplete multivariate genetic variance, but that sexual conflict over insemination success may oppose this loss of variance. We suggest that changes in the direction of selection due to sexually antagonistic interactions will be an important and potentially widespread factor in maintaining multivariate genetic variation.     

EPISTASIS AND THE EVOLUTION OF ADDITIVE GENETIC VARIANCE IN POPULATIONS THAT PASS THROUGH A BOTTLENECK

Traditional models of genetic drift predict a linear decrease in additive genetic variance for populations passing through a bottleneck. This perceived lack of heritable variance limits the scope of founder-effect models of speciation. We produced 55 replicate bottleneck populations maintained at two male-female pairs through four generations of inbreeding (average F = 0.39). These populations were formed from an F₂ intercross of the LG/J and SM/J inbred mouse strains. Two contemporaneous control strains maintained with more than 60 mating pairs per generation were formed from this same source population. The average level of within-strain additive genetic variance for adult body weight was compared between the control and experimental lines. Additive genetic variance for adult body weight within experimental bottleneck strains was significantly higher than expected under an additive genetic model This enhancement of additive genetic variance under inbreeding is likely to be due to epistasis, which retards or reverses the loss of additive genetic variance under inbreeding for adult body weight in this population. Therefore, founder-effect speciation processes may not be constrained by a loss of heritable variance due to population bottlenecks.     

SEX AND SPECIATION: GENETIC ARCHITECTURE AND EVOLUTIONARY POTENTIAL OF SEXUAL VERSUS NONSEXUAL TRAITS IN THE SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX

Phenotypic divergence in the male reproductive system (genitalia and gonads) between species of the Drosophila melanogaster complex and their hybrids was quantified to decipher the role of these traits in species differentiation and speciation. Internal as well as external, sexual and nonsexual traits were analyzed with respect to genetic variation and trait asymmetry between strains within species, genetic divergence between species, and dominance and asymmetry in species and hybrids. The variation between strains within species was significant among sexual traits, and only external traits were less asymmetric than internal ones, which suggests that sexual traits are not strongly constrained within species. Three main findings show that sexual traits are most divergent between species: (1) testis length and area, and the area of the posterior lobe of the genital arch (sexual traits) showed the highest proportion of variation between species; (2) linear discriminant functions with the highest components associated to sexual traits were better predictors of species membership; and (3) testis length and area revealed a departure from a linear relationship between members of the species group. Examination of interspecific hybrids showed that sexual traits had higher asymmetry in species hybrids than in the parental species and that sexual traits showed additivity or dominance whereas nonsexual traits showed overdominance (with the exception of malpighian tubules length). These results suggest that sexual traits have undergone more genetic changes and, as a result, tend to show higher divergence and stronger hybrid breakdown between species than nonsexual traits. We propose that sexual selection in the broad sense, affecting all aspects of sexuality, may be responsible for the diversified appearance of sexual traits among closely related species and that the genetic architecture underlying sexual traits may be more prone to disruption during the early stages of speciation.     

QUANTITATIVE GENETIC DIVERGENCE AND STANDING GENETIC (CO)VARIANCE IN THERMAL REACTION NORMS ALONG LATITUDE

Although the potential to adapt to warmer climate is constrained by genetic trade‐offs, our understanding of how selection and mutation shape genetic (co)variances in thermal reaction norms is poor. Using 71 isofemale lines of the fly Sepsis punctum, originating from northern, central, and southern European climates, we tested for divergence in juvenile development rate across latitude at five experimental temperatures. To investigate effects of evolutionary history in different climates on standing genetic variation in reaction norms, we further compared genetic (co)variances between regions. Flies were reared on either high or low food resources to explore the role of energy acquisition in determining genetic trade‐offs between different temperatures. Although the latter had only weak effects on the strength and sign of genetic correlations, genetic architecture differed significantly between climatic regions, implying that evolution of reaction norms proceeds via different trajectories at high latitude versus low latitude in this system. Accordingly, regional genetic architecture was correlated to region‐specific differentiation. Moreover, hot development temperatures were associated with low genetic variance and stronger genetic correlations compared to cooler temperatures. We discuss the evolutionary potential of thermal reaction norms in light of their underlying genetic architectures, evolutionary histories, and the materialization of trade‐offs in natural environments.     

GENETIC REGULATORY NETWORK MOTIFS CONSTRAIN ADAPTATION THROUGH CURVATURE IN THE LANDSCAPE OF MUTATIONAL (CO)VARIANCE

Systems biology is accumulating a wealth of understanding about the structure of genetic regulatory networks, leading to a more complete picture of the complex genotype–phenotype relationship. However, models of multivariate phenotypic evolution based on quantitative genetics have largely not incorporated a network‐based view of genetic variation. Here we model a set of two‐node, two‐phenotype genetic network motifs, covering a full range of regulatory interactions. We find that network interactions result in different patterns of mutational (co)variance at the phenotypic level (the M ‐matrix), not only across network motifs but also across phenotypic space within single motifs. This effect is due almost entirely to mutational input of additive genetic (co)variance. Variation in M has the effect of stretching and bending phenotypic space with respect to evolvability, analogous to the curvature of space–time under general relativity, and similar mathematical tools may apply in each case. We explored the consequences of curvature in mutational variation by simulating adaptation under divergent selection with gene flow. Both standing genetic variation (the G ‐matrix) and rate of adaptation are constrained by M , so that G and adaptive trajectories are curved across phenotypic space. Under weak selection the phenotypic mean at migration‐selection balance also depends on M .     

EPISTASIS AND THE INCREASE IN ADDITIVE GENETIC VARIANCE: IMPLICATIONS FOR PHASE 1 OF WRIGHT'S SHIFTING-BALANCE PROCESS

Central to Wright's shifting-balance theory is the idea that genetic drift and selection in systems with gene interaction can lead to the formation of “adaptive gene complexes.” The theory of genetic drift has been well developed over the last 60 years; however, nearly all of this theory is based on the assumption that only additive gene effects are acting. Wright's theory was developed recognizing that there was a “universality of interaction effects,” which implies that additive theory may not be adequate to describe the process of differentiation that Wright was considering. The concept of an adaptive gene complex implies that an allele that is favored by individual selection in one deme may be removed by selection in another deme. In quantitative genetic terms, the average effects of an allele relative to other alleles changes from deme to deme. The model presented here examines the variance in local breeding values (LBVs) of a single individual and the covariance in the LBVs of a pair of individuals mated in the same deme relative to when they are mated in different demes. Local breeding value is a measure of the average effects of the alleles that make up that individual in a particular deme. I show that when there are only additive effects the covariance between the LBVs of individuals equals the variance in the LBV of an individual. As the amount of epistasis in the ancestral population increases, the variance in the LBV of an individual increases and the covariance between the LBVs of a pair of individuals decreases. The divergence in these two values is a measure of the extent to which the LBV of an individual varies independently of the LBVs of other individuals. When this value is large, it means that the relative ordering of the average effects of alleles will change from deme to deme. These results confirm an important component of Wright's shifting-balance theory: When there is gene interaction, genetic drift can lead to the reordering of the average effects of alleles and when coupled with selection this will lead to the formation of the adaptive gene complexes.     

EVOLUTION IN FLUCTUATING ENVIRONMENTS: DECOMPOSING SELECTION INTO ADDITIVE COMPONENTS OF THE ROBERTSON–PRICE EQUATION

We analyze the stochastic components of the Robertson–Price equation for the evolution of quantitative characters that enables decomposition of the selection differential into components due to demographic and environmental stochasticity. We show how these two types of stochasticity affect the evolution of multivariate quantitative characters by defining demographic and environmental variances as components of individual fitness. The exact covariance formula for selection is decomposed into three components, the deterministic mean value, as well as stochastic demographic and environmental components. We show that demographic and environmental stochasticity generate random genetic drift and fluctuating selection, respectively. This provides a common theoretical framework for linking ecological and evolutionary processes. Demographic stochasticity can cause random variation in selection differentials independent of fluctuating selection caused by environmental variation. We use this model of selection to illustrate that the effect on the expected selection differential of random variation in individual fitness is dependent on population size, and that the strength of fluctuating selection is affected by how environmental variation affects the covariance in Malthusian fitness between individuals with different phenotypes. Thus, our approach enables us to partition out the effects of fluctuating selection from the effects of selection due to random variation in individual fitness caused by demographic stochasticity.     

EVOLUTION OF FLORAL TRAITS IN A HERMAPHRODITIC PLANT: FIELD MEASUREMENTS OF HERITABILITIES AND GENETIC CORRELATIONS

Genetic variances, heritabilities, and genetic correlations of floral traits were measured in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae). A paternal half-sib design was employed to generate seeds in each of four years, and seeds were planted back in the field near the parental site. The progeny were followed for up to eight years to estimate quantitative genetic parameters subject to natural levels of environmental variation over the entire life cycle. Narrow-sense heritabilities of 0.2–0.8 were detected for the morphometric traits of corolla length, corolla width, stigma position, and anther position. The proportion of time spent by the protandrous flowers in the pistillate phase (“proportion pistillate”) also exhibited detectable heritability of near 0.3. In contrast, heritability estimates for nectar reward traits were low and not significantly different from zero, due to high environmental variance between and within flowering years. The estimates of genetic parameters were combined with phenotypic selection gradients to predict evolutionary responses to selection mediated by the hummingbird pollinators. One trait, corolla width, showed the potential for a rapid response to ongoing selection through male function, as it experienced both direct selection, by influencing pollen export, and relatively high heritability. Predicted responses were lower for proportion pistillate and corolla length, even though these traits also experienced direct selection. Stigma position was expected to respond positively to indirect selection of proportion pistillate but negatively to selection of corolla length, with the net effect sensitive to variation in the selection estimates. Anther position also was not directly selected but could respond to indirect selection of genetically correlated traits.     

SEED SET AND SEED MASS IN IPOMOPSIS AGGREGATA: VARIANCE PARTITIONING AND INFERENCES ABOUT POSTPOLLINATION SELECTION

Events that follow pollination, such as pollen-tube growth and seed maturation, comprise an important phase of angiosperm reproduction. Differential success during this “postpollination” phase may represent phenotypic selection, including sexual selection, or interaction between parents caused, for example, by their genetic similarity. By providing a detailed partitioning of variance in success, diallel crossing designs offer great potential to determine which processes are occurring and their relative magnitudes. We performed three partial diallels with the montane herb Ipomopsis aggregata, using a large sample of parental plants (69 total). Embedded in the designs were crossing-distance treatments of 1 m, 10 m, and 100 m, reflecting a range of parental genetic similarity. We partitioned phenotypic variance in seed set per fruit into six components using restricted maximum-likelihood (REML) analysis. For one diallel, we also partitioned variance in seed mass into five components, and estimated two components of covariance between seed set and mass. Variance caused by maternal effects (V_mat) comprised 12%–35% of total variance in seed set and 62% of variance in seed mass, and there was a significant negative environmental covariance between seed set and seed mass. Parental interaction made no detectable contribution to phenotypic variance in either of our measures of postpollination success, although crossing distance did contribute slightly but significantly to fit of the model in some cases. Finally, there was no detectable paternal variance (V_pat) in seed set or seed mass. These results are in keeping with reports from other studies of natural plant populations. The finding of little or no paternal variance in particular suggests little scope for postpollination sexual selection through the male function of cosexual plants such as I. aggregata.     

THE EVOLUTION OF SOCIAL SIGNALS: MORPHOLOGICAL,FUNCTIONAL, AND GENETIC INTEGRATION OF THE SEX PHEROMONE IN NAUPHOETA CINEREA

Social signals that mediate intraspecific interactions can be complex, conveying considerable information concerning the probable behavior of individuals and minimizing overt aggression and wasted energy. In the cockroach Nauphoeta cinerea, male-male competition and female mate choice are mediated by a multicomponent male-produced sex pheromone. In this study, I examine variation in this pheromone. First I measure differences among males in both individual pheromone compounds and the overall composition of the pheromone. Principal component analysis is used to quantify and describe pheromone composition. Next, I explore some of the causes and consequences of this variation by examining the pheromone of males with different social experiences. Compared to subordinate males, dominant males have significantly less variable quantities of the individual pheromone compounds and are significantly less variable in the composition of their pheromone. Because of an association between status and mating success, male-male competition can result in stabilizing sexual selection on the sex pheromone. Finally, I test the hypothesis that the pheromone compounds evolve in a manner consistent with their function. As predicted for morphologically integrated characters, the patterns of phenotypic, genetic, and environmental correlations among my measures of pheromone compounds and composition match functional patterns suggested by this study and the developmental patterns demonstrated in my previous studies. Based on these studies of the N. cinerea sex pheromone, I argue that stabilizing sexual selection shapes the evolution of pheromonal communication involved in social interactions among male N. cinerea. Further, I argue that coordinated evolution of social signals may be possible due to the morphological integration of their multiple compounds.     

EVOLUTION OF RESISTANCE TO A MULTIPLE‐HERBIVORE COMMUNITY: GENETIC CORRELATIONS,DIFFUSE COEVOLUTION,AND CONSTRAINTS ON THE PLANT'S RESPONSE TO SELECTION

Although plants are generally attacked by a community of several species of herbivores, relatively little is known about the strength of natural selection for resistance in multiple‐herbivore communities—particularly how the strength of selection differs among herbivores that feed on different plant organs or how strongly genetic correlations in resistance affect the evolutionary responses of the plant. Here, we report on a field study measuring natural selection for resistance in a diverse community of herbivores of Solanum carolinense. Using linear phenotypic‐selection analyses, we found that directional selection acted to increase resistance to seven species. Selection was strongest to increase resistance to fruit feeders, followed by flower feeders, then leaf feeders. Selection favored a decrease in resistance to a stem borer. Bootstrapping analyses showed that the plant population contained significant genetic variation for each of 14 measured resistance traits and significant covariances in one‐third of the pairwise combinations of resistance traits. These genetic covariances reduced the plant's overall predicted evolutionary response for resistance against the herbivore community by about 60%. Diffuse (co)evolution was widespread in this community, and the diffuse interactions had an overwhelmingly constraining (rather than facilitative) effect on the plant's evolution of resistance.     

CONDITION DEPENDENCE OF A SEXUALLY SELECTED TRAIT IN A CRUSTACEAN SPECIES COMPLEX: IMPORTANCE OF THE ECOLOGICAL CONTEXT

The genic capture model offers a promising solution to the lek paradox. Heightened condition dependency of sexually selected traits is a prerequisite of this model. Condition dependency is empirically inferred by the sensitivity of traits to stressors. The magnitude of ecological stress (e.g., competition and predation) experienced by populations varies considerably. Thus, condition dependence should manifest more in populations experiencing higher levels of stress. We experimentally assessed the sensitivity of a sexually selected trait (posterior gnathopod) to food resource stress in an amphipod species. We found that gnathopod size variation was 59% higher under food stress, with no corresponding effect on nonsexually selected traits. In addition, we assessed levels of gnathopod variation and the allometry of gnathopods for males sampled from natural populations for two amphipod species that experience different levels of stress (driven by contrasting size‐selective predation and associated life‐history trade‐offs). Populations that experience higher resource stress had both steeper allometries and greater gnathopod size variation. These results suggest that the magnitude of ecological stress experienced by natural populations strongly impacts condition dependency of sexually selected traits, and could play an important role in shaping trait variation and thus the opportunity for sexual selection.     

FLUCTUATING SELECTION AND THE MAINTENANCE OF INDIVIDUAL AND SEX‐SPECIFIC DIET SPECIALIZATION IN FREE‐LIVING OYSTERCATCHERS

Fluctuating and disruptive selection are important mechanisms for maintaining intrapopulation trait variation. Nonetheless, few field studies quantify selection pressures over long periods and identify what causes them to fluctuate. Diet specialists in oystercatchers differ in short‐term payoffs (intake), but their long‐term payoffs are hypothesized to be condition dependent. We test whether phenotypic selection on diet specialization fluctuates between years due to the frequency of specialists, competitor density, prey abundance, and environmental conditions. Short‐term payoffs proved to be poor predictors of long‐term fitness payoffs of specialization. Sex‐differences in diet specialization were maintained by opposing directional fecundity and viability selection between the sexes. Contrasting other studies, selection on individual diet specialization was neither negative frequency‐ or density‐dependent nor dependent on prey abundance. Notwithstanding, viability selection fluctuated strongly (stabilizing?disruptive) over the 26‐year study period: slightly favoring generalists in most years, but strongly disfavoring generalists in rare harsh winters, suggesting generalists cannot cope with extreme conditions. Although selection fluctuated, mean selection on specialists was weak, which can explain how individual specialization can persist over long periods. Because rare events can dramatically affect long‐term selective landscapes, more care should be taken to match the timescale of evolutionary studies to the temporal variability of critical environmental conditions.     

THE INTERPLAY BETWEEN LOCAL ECOLOGY,DIVERGENT SELECTION,AND GENETIC DRIFT IN POPULATION DIVERGENCE OF A SEXUALLY ANTAGONISTIC FEMALE TRAIT

Genetically polymorphic species offer the possibility to study maintenance of genetic variation and the potential role for genetic drift in population divergence. Indirect inference of the selection regimes operating on polymorphic traits can be achieved by comparing population divergence in neutral genetic markers with population divergence in trait frequencies. Such an approach could further be combined with ecological data to better understand agents of selection. Here, we infer the selective regimes acting on a polymorphic mating trait in an insect group; the dorsal structures (either rough or smooth) of female diving beetles. Our recent work suggests that the rough structures have a sexually antagonistic function in reducing male mating attempts. For two species (Dytiscus lapponicus and Graphoderus zonatus), we could not reject genetic drift as an explanation for population divergence in morph frequencies, whereas for the third (Hygrotus impressopunctatus) we found that divergent selection pulls morph frequencies apart across populations. Furthermore, population morph frequencies in H. impressopunctatus were significantly related to local bioclimatic factors, providing an additional line of evidence for local adaptation in this species. These data, therefore, suggest that local ecological factors and sexual conflict interact over larger spatial scales to shape population divergence in the polymorphism.     

BRINGING HABITAT INFORMATION INTO STATISTICAL TESTS OF LOCAL ADAPTATION IN QUANTITATIVE TRAITS: A CASE STUDY OF NINE‐SPINED STICKLEBACKS

Detection of footprints of historical natural selection on quantitative traits in cross‐sectional data sets is challenging, especially when the number of populations to be compared is small and the populations are subject to strong random genetic drift. We extend a recent Bayesian multivariate approach to differentiate between selective and neutral causes of population differentiation by the inclusion of habitat information. The extended framework allows one to test for signals of selection in two ways: by comparing the patterns of population differentiation in quantitative traits and in neutral loci, and by comparing the similarity of habitats and phenotypes. We illustrate the framework using data on variation of eight morphological and behavioral traits among four populations of nine‐spined sticklebacks (Pungitius pungitius). In spite of the strong signal of genetic drift in the study system (average F_ST = 0.35 in neutral markers), strong footprints of adaptive population differentiation were uncovered both in morphological and behavioral traits. The results give quantitative support for earlier qualitative assessments, which have attributed the observed differentiation to adaptive divergence in response to differing ecological conditions in pond and marine habitats.     

SEXUAL CONFLICT AND INTERACTING PHENOTYPES: A QUANTITATIVE GENETIC ANALYSIS OF FECUNDITY AND COPULA DURATION IN DROSOPHILA MELANOGASTER

Many reproductive traits that have evolved under sexual conflict may be influenced by both sexes. Investigation of the genetic architecture of such traits can yield important insight into their evolution, but this entails that the heritable component of variation is estimated for males and females—as an interacting phenotype. We address the lack of research in this area through an investigation of egg production and copula duration in the fruit fly, Drosophila melanogaster. Despite egg production rate being determined by both sexes, which may cause sexual conflict, an assessment of this trait as an interacting phenotype is lacking. It is currently unclear whether copula duration is determined by males and/or females. We found significant female, but not male, genetic variance for egg production rate that may indicate reduced potential for ongoing sexually antagonistic coevolution. In contrast, copula duration was determined by significant genetic variance in both sexes. We also identified genetic variation in egg retention among virgin females. Although previously identified in wild populations, it is unclear why this should be present in a laboratory stock. This study provides a novel insight into the shared genetic architecture of reproductive traits that are the subject of sexual conflict.     

MAINTENANCE OF GENETIC VARIATION IN HUMAN PERSONALITY: TESTING EVOLUTIONARY MODELS BY ESTIMATING HERITABILITY DUE TO COMMON CAUSAL VARIANTS AND INVESTIGATING THE EFFECT OF DISTANT INBREEDING

Personality traits are basic dimensions of behavioral variation, and twin, family, and adoption studies show that around 30% of the between‐individual variation is due to genetic variation. There is rapidly growing interest in understanding the evolutionary basis of this genetic variation. Several evolutionary mechanisms could explain how genetic variation is maintained in traits, and each of these makes predictions in terms of the relative contribution of rare and common genetic variants to personality variation, the magnitude of nonadditive genetic influences, and whether personality is affected by inbreeding. Using genome‐wide single nucleotide polymorphism (SNP) data from > 8000 individuals, we estimated that little variation in the Cloninger personality dimensions (7.2% on average) is due to the combined effect of common, additive genetic variants across the genome, suggesting that most heritable variation in personality is due to rare variant effects and/or a combination of dominance and epistasis. Furthermore, higher levels of inbreeding were associated with less socially desirable personality trait levels in three of the four personality dimensions. These findings are consistent with genetic variation in personality traits having been maintained by mutation–selection balance.