Academic journal article Genetics

Dominance Genetic Variance for Traits under Directional Selection in Drosophila Serrata

Academic journal article Genetics

Dominance Genetic Variance for Traits under Directional Selection in Drosophila Serrata

Article excerpt

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CHARACTERIZING the genetic basis of phenotypes and the form and resulting consequences of selection on these phenotypes is a major goal of evolutionary biology. Substantial effort has been devoted to estimating additive genetic variance in metric traits and fitness components (Falconer and Mackay 1996; Lynch and Walsh 1998), establishing that the majority of metric traits have additive genetic variance and a heritability in the range of 0.2-0.6 (Lynch and Walsh 1998). More recently, the necessity of examining multivariate patterns of additive genetic variance and selection has been emphasized (Walsh and Blows 2009) and shown to influence the multivariate response to selection in laboratory (e.g., Mezey and Houle 2005; McGuigan and Blows 2009; Hine et al. 2014) and natural populations (Clements et al. 2011; Morrissey et al. 2012). In particular, additive genetic variance in all single traits often does not equate to genetic variance in all multivariate trait combinations (Hine and Blows 2006; Blows 2007; Walsh and Blows 2009), and a response to selection in trait combinations with low levels of additive genetic variance may be stochastic in nature (Hine et al. 2014).

In contrast to our growing understanding of patterns of additive genetic variance, very little is known about the relative contributions of nonadditive variance, particularly dominance variance, to multivariate phenotypes, despite the ubiquity of dominance and the attention given to the evolution of dominance for close to a century (Fisher 1928; Wright 1929; Wright 1934). The pervasiveness of dominance is demonstrated most clearly by inbreeding depression (Charlesworth and Charlesworth 1987), which is exhibited in almost all organisms to some degree (Husband and Schemske 1996; Lynch and Walsh 1998). The increased frequency of homozygous loci across the genome, caused by inbreeding, exposes recessive deleterious alleles that are typically held in a heterozygous state, resulting in the decrease in trait means, and initial fitness reductions that accompany inbreeding (Lande and Schemske 1985; Lynch 1991; Charlesworth et al. 1999). Similarly, selection for recessive deleterious alleles in heterozygotes results in the typically faster responses observed for downward than upward artificial selection, when the dominant allele confers a higher trait mean than the recessive (Falconer and Mackay 1981).

Remarkably high levels of inbreeding depression, averaging 50%, have been demonstrated for primary fitness components (e.g., viability, fertility, egg production) in Drosophila, compared to levels of a few percent for morphological traits (Lynch and Walsh 1998), and asymmetric selection responses for fitness components have also been demonstrated in several cases (Frankham 1990). These observations are consistent with predicted patterns of dominance genetic variance for traits that are genetically correlated with fitness (Fisher 1930; Frankham 1990; Crnokrak and Roff 1995). Directional selection on fitnesscorrelated traits is expected to erode the additive genetic variance in these traits (Fisher 1930), resulting in lower heritabilites (Mousseau and Roff 1987; Price and Schluter 1991; Kruuk et al. 2000) and a higher proportion of dominance variance contributing to overall phenotypic variance (Merilä and Sheldon 1999). Consequently, fitness itself, a trait unambiguously under directional selection, is predicted to have the least additive and proportionately largest contribution of dominance variance to phenotypic variance. In addition to single traits, particular multivariate combinations of traits known to be under persistent directional selection through their association with sexual fitness have been demonstrated to have low additive genetic variance (McGuigan and Blows 2009; Hine et al. 2011; Sztepanacz and Rundle 2012), suggesting that similar patterns of additive and dominance contributions to phenotypic variance may also be observed for multivariate traits in certain circumstances. …

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