Simultaneous Estimation of Additive and Mutational Genetic Variance in an Outbred Population of Drosophila serrata

Abstract

How new mutations contribute to genetic variation is a key question in biology. Although the evolutionary fate of an allele is largely determined by its heterozygous effect, most estimates of mutational variance and mutational effects derive from highly inbred lines, where new mutations are present in homozygous form. In an attempt to overcome this limitation, middle-class neighborhood (MCN) experiments have been used to assess the fitness effect of new mutations in heterozygous form. However, because MCN populations harbor substantial standing genetic variance, estimates of mutational variance have not typically been available from such experiments. Here we employ a modification of the animal model to analyze data from 22 generations of Drosophila serrata bred in an MCN design. Mutational heritability, measured for eight cuticular hydrocarbons, 10 wing-shape traits, and wing size in this outbred genetic background, ranged from 0.0006 to 0.006 (with one exception), a similar range to that reported from studies employing inbred lines. Simultaneously partitioning the additive and mutational variance in the same outbred population allowed us to quantitatively test the ability of mutation-selection balance models to explain the observed levels of additive and mutational genetic variance. The Gaussian allelic approximation and house-of-cards models, which assume real stabilizing selection on single traits, both overestimated the genetic variance maintained at equilibrium, but the house-of-cards model was a closer fit to the data. This analytical approach has the potential to be broadly applied, expanding our understanding of the dynamics of genetic variance in natural populations.

Mutation Is a Sufficient and Robust Predictor of Genetic Variation for Mitotic Spindle Traits in Caenorhabditis elegans

“…Probably the most comparable data to ours in terms of the types of traits are from D. serrata, in which McGuigan et al (2015) report VG and VM for eight cuticular hydrocarbons and 10 wing dimensions. The median t P was 125 generations, again suggestive of substantially stronger selection against homozygotes.…”

“…Fruit flies are obligate outcrossers, so selection against new mutations occurs primarily in heterozygotes, which implies that selection against mutant homozygotes must be substantially stronger. Persistence times of heterozygous mutations affecting life history traits in Daphnia are similar to those in D. melanogaster, on the order of 40 generations (Lynch et al 1998).Probably the most comparable data to ours in terms of the types of traits are from D. serrata, in which McGuigan et al (2015) report VG and VM for eight cuticular hydrocarbons and 10 wing dimensions. The median t P was 125 generations, again suggestive of substantially stronger selection against homozygotes.…”

“…Second, when scaled relative to the trait mean, life history traits experience greater input of genetic variation from mutation than other classes of traits (Houle et al 1996;Halligan and Keightley 2009). Third, life history traits appear to be under stronger purifying selection than other classes of traits (Houle et al 1996;Lynch et al 1999;McGuigan et al 2015).A longstanding related, but unanswered, question is the relative influence of balancing selection on the maintenance of genetic variation (Dobzhansky 1955;Lewontin 1974; Charlesworth 2015). Presumably, a large fraction of mutations are unconditionally deleterious and are removed more or less efficiently by selection.…”

“…Second, when scaled relative to the trait mean, life history traits experience greater input of genetic variation from mutation than other classes of traits (Houle et al 1996;Halligan and Keightley 2009). Third, life history traits appear to be under stronger purifying selection than other classes of traits (Houle et al 1996;Lynch et al 1999;McGuigan et al 2015).…”

Cross‐sex genetic covariances limit the evolvability of wing‐shape within and among species of Drosophila

“…Pleiotropy produces covariation among traits, orienting new genetic variation that arises from mutation (Houle and Fierst ; McGuigan et al. ; Hine et al. ), and standing genetic variation (Walsh and Blows ), into a smaller number of multivariate trait combinations.…”