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Dominance Variance: Associations with Selection and Fitness

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Dominance Variance: Associations with Selection and Fitness Heredity 75(1995) 530—540 Received24Apr11 1995 Dominance variance: associations with selection and fitness PETER CRNOKRAK* & DEREK A. ROFF Department of Biology, McGill University, 1205 Dr. Pen field Avenue, Montreal, Quebec, Canada H3A lB 1 Strongdirectional, and to some degree stabilizing, selection usually erodes only additive genetic variance while not affecting dominance variance. Consequently, traits closely associated with fitness should exhibit high levels of dominance variance. In this study we compile a large number of estimates of dominance variance to determine if traits that are subject to strong selection and/or are closely associated with fitness have higher levels of dominance variance than traits less subject to selection pressure. Estimates were taken from the literature for both wild and domestic species and each group was treated separately. Traits closely associated with fitness (life history) had significantly higher dominance components than did traits more distantly related to fitness (morphology) for wild species. No significant differences were found between life history and morphological traits for domestic species. Traits that were known to have been subject to intense directional selection (morphological traits for domestic species) had significantly higher dominance estimates than did traits that were assumed not to have been subject to strong selection (morphological traits for wild outbred species). The results are discussed with respect to the maintenance of heritable variation and the bias introduced in the calculation of the full-sib heritability estimate by high levels of dominance variance. Keywords:dominancevariance, fitness, genetic variation, selection. Introduction agree that traits closely associated with fitness should exhibit high levels of dominance variance. Thegenetic architecture of a quantitative trait is Despite this, few studies have examined the preva- composed of additive (Va), dominance (Vd), epistatic lence of dominance variance in traits of evolutionary (Vj) variance and interactions of all three compo- significance and how selection influences the level of nents (Bulmer, 1985). Of most importance to the dominance for traits closely and more distantly transmission of a trait from one generation to the related to fitness. next and for predicting the short-term response to Strong directional selection (and to a lesser selection is the narrow sense heritability, h2, the degree, stabilizing selection; Lee & Parsons, 1968; ratio of additive variance to phenotypic variance. Lacy, 1987) is predicted to erode additive genetic Dominance variance is generally not considered variance and, subsequently, decrease the heritability important as it does not predict the response to of a trait (Felsenstein, 1965; Lande, 1988; Turelli, selection (Fisher, 1930; Lynch, 1994). However, 1988; Gomez-Raya & Burnside, 1990; Villanueva & dominance variance can affect the heritability of Kennedy, 1990; references in Arnold, 1990 and Gar- traits during bottleneck events where nonadditive land & Bennett, 1990; for a review see Rose et al., genetic variance (both dominance and epistatic) can 1987). As a consequence, the response to selection be 'converted' into or affect additive genetic vari- will be reduced (but the reduction in response may ance and therefore become available for selection to result from other factors: see Falconer (1989) and act upon (for a review see Carson, 1990). General Lande (1988)). Traits for a population at equi- patterns of dominance variance have been predicted librium are predicted to have low additive genetic by a number of theoreticians (Lynch, 1994); variance as it is assumed that selection has moulded although mechanisms of the evolution of genetic them to an optimum (Hegmann & Dingle, 1982; dominance are different among the theories, all Lynch & Sulzbach, 1984; but see Charlesworth (1987) for an alternative explanation). Because they *Correspondence. are assumed to be subject to intense selection, traits 530 1995The Genetical Society of Great Britain. DOMINANCE VARIANCE: SELECTION AND FITNESS 531 most closely associated with fitness are predicted to cerning the relative distribution of dominance vari- have low heritabilities and subsequently relatively ance across traits that are associated with fitness high dominance components (Wright, 1929; Hal- and/or subject to selection to different degrees. dane, 1932; Lerner, 1954; Fisher, 1958). A number The present study addresses two main questions. of studies (Mousseau & Roff, 1987; Roff & Mous- (i) How does the relative contribution of dominance seau, 1987; Garland et al., 1990; Willis et a!., 1991; variance change from one trait-type to another? Do Partridge, 1994) have shown that life history traits, traits that are closely associated with fitness have which are assumed to be closely connected to fit- relatively high levels of Vd as predicted from theory? ness, have low heritabilities while morphological (ii) Do patterns of Vd change from wild outbred traits, which are assumed to be more distantly species to domestic species for particular trait cate- relatedtofitness,have highheritabilities gories? Although we have no studies that have (behavioural and physiological traits are usually examined what changes occur in the genetic archi- intermediate to the above two types of traits). tecture of a trait in the presence of selection for a Because selection usually erodes only additive wide variety of traits and species, the above com- genetic variance (Lynch, 1994), although changes in parison will allow us at least to speculate how strong gene frequency may also cause changes in nonaddi- directional selection can change the relative con- tive variance as well, one would predict that the tribution of Va and Vd to the genetic variance of a opposite pattern should be found in terms of domi- trait. nance variance: life history traits should have rela- tively high levels of dominance variance while morphological traits should have low levels of domi- Materials and methods nance variance. In addition to eroding additive vari- Estimates of dominance variance ance, selection is also expected to act directly on genetic dominance, resulting in a further relative Three hundred and thirty-eight estimates of domi- increase of dominance variance to total genetic vari- nance variance were obtained from 55 sources; 17 ance (Mather, 1979; Lynch, 1994). Fisher's (1958) wild outbred species and 21 domestic species. theory predicts that dominance will evolve in both Species were classified as domestic if they had been magnitude and direction of increasing fitness. subject to long-term deliberate artificial selection Although Fisher's theory of the evolution of domi- and usually included species of economic impor- nance has been strongly criticized (for a review see tance such as Zea mays. The relative contribution of Charlesworth, 1979), empirical investigations have dominance variance to the genetic variance of a trait confirmed the last point (Breese & Mather; 1960; was calculated in two ways: (i) dominance variance Kearsey & Kojima, 1967; Lynch, 1994 and refer- as a function of the sum of dominance and additive ences therein). On a per species basis, few studies variance: exist that have examined changes that occur as a V result of selection acting on the genetic architecture D = d of quantitative traits. For the most part, strong Vd+Va selection does decrease additive variance and, in most cases, heritability, although in some cases the and (ii) dominance variance as a function of pheno- decreases are relatively small (Kaufman et a!., 1977; typic variance: Enfield, 1980). Discrete traits such as dimorphisms Vd that are controlled by some underlying normally dis- — tributed variable, when subject to strong directional Vp selection may not experience an appreciable decrease in genetic variance because the intensity of Thevariable Da was used to assess the relative con- selection declines very quickly over time (Roff, tributions of dominance and additive variances irre- 1994). spective of the phenotypic variance for a trait. Short compilations have been made of patterns of Although selection may affect V (Hayashi & Ukai, dominance and nonadditive variance in the past but 1994), most interest lies in how it affects the genetic these have been either qualitative (Kearsey & architecture of a trait. Nevertheless, a high level of Kojima, 1967) or have reported quantitative results Vd may be inconsequential to a trait if it is small of only a few traits for a few species (see Garland, compared with V; for this reason, we also used the 1994 for a review). This study is the first to attempt variable D. Negative variance estimates reported in a compilation of a large number of estimates con- the literature were standardized to zero (Kendall & The Genetical Society of Great Britain, Heredity, 75, 530—540. 532 P. CRNOKRAK & D. A. ROFF Stuart, 1979). We obtained 232 estimates of D and 1981, table 10.1, p. 150; Mousseau & Roff, 1987) 106 estimates of D. For those studies that reported investigations concerning the relationship between more than one estimate of dominance variance for fitness and heritability estimates, one would expect each trait (repeated trials or measures under dif- that behavioural and physiological traits should fall ferent conditions) we used the mean. A list of between life history and morphological traits (Roff species, estimates and references is available from & Mousseau, 1987). For behavioural traits at least, the corresponding
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