Genetic architecture of fitness and nonfitness traits: Empirical patterns and development of ideas

Abstract

Comparative studies of the genetic architecture of different types of traits were initially prompted by the expectation that traits under strong directional selection (fitness traits) should have lower levels of genetic variability than those mainly under weak stabilizing selection (nonfitness traits). Hence, early comparative studies revealing lower heritabilities of fitness than nonfitness traits were first framed in terms of giving empirical support for this prediction, but subsequent treatments have effectively reversed this view. Fitness traits seem to have higher levels of additive genetic variance than nonfitness traits - an observation that has been explained in terms of the larger number loci influencing fitness as compared to nonfitness traits. This hypothesis about the larger functional architecture of fitness than nonfitness traits is supported by their higher mutational variability, which is hard to reconcile without evoking capture of mutational variability over many loci. The lower heritabilities of fitness than nonfitness traits, despite the higher additive genetic variance of the former, occur because of their higher residual variances. Recent comparative studies of dominance contributions for different types of traits, together with theoretical predictions and a large body of indirect evidence, suggest an important role of dominance variance in determining levels of residual variance for fitness-traits. The role of epistasis should not be discounted either, since a large number of loci increases the potential for epistatic interactions, and epistasis is strongly implicated in hybrid breakdown.