Evolutionary optimum for male sexual traits characterized using the multivariate Robertson–Price Identity

Abstract

Phenotypes tend to remain relatively constant in natural populations, suggesting a limit to trait evolution. Although stationary phenotypes suggest stabilizing selection, directional selection is more commonly reported. However, selection on phenotypes will have no evolutionary consequence if the traits do not genetically covary with fitness, a covariance known as the Robertson-Price Identity. The nature of this genetic covariance determines if phenotypes will evolve directionally or whether they reside at an evolutionary optimum. Here, we show how a set of traits can be shown to be under net stabilizing selection through an application of the multivariate Robertson-Price Identity. We characterize how a suite of male sexual displays genetically covaries with fitness in a population of Drosophila serrata. Despite strong directional sexual selection on these phenotypes directly and significant genetic variance in them, little genetic covariance was detected with overall fitness. Instead, genetic analysis of trait deviations showed substantial stabilizing selection on the genetic variance of these traits with respect to overall fitness, indicating that they reside at an evolutionary optimum. In the presence of widespread pleiotropy, stabilizing selection on focal traits will arise through the net effects of selection on other, often unmeasured, traits and will tend to be stronger on trait combinations than single traits. Such selection may be difficult to detect in phenotypic analyses if the environmental covariance between the traits and fitness obscures the underlying genetic associations. The genetic analysis of trait deviations provides a way of detecting the missing stabilizing selection inferred by recent metaanalyses. cuticular hydrocarbons | evolutionary stasis

Dominance Genetic Variance for Traits Under Directional Selection inDrosophila serrata

“…The D. serrata population used here was maintained on a laboratory transfer schedule, in which adult lifespan is only a few days once sexual maturity is reached, for 50 generations prior to this experiment. Our fitness assay was, therefore, designed to capture the significant components of fitness under these conditions and was similar to other assays that have been used to characterize fitness in D. serrata (e.g., Delcourt et al 2012;Reddiex et al 2013;Collet and Blows 2014). In this species, female remating rates are among the highest in Drosophila, with previous evidence indicating that during 48 hr of mating opportunities a single female will produce offspring from 2.9 sires, on average (Frentiu and Chenoweth 2008).…”

“…Therefore, our measure of fitness was comprehensive, including a male's mating success, the productivity of the female he mated to, and the survival to emergence of his offspring, and it was within a competitive arena that is likely to occur in nature (Frentiu and Chenoweth 2008). Low additive genetic variance for net fitness has also been demonstrated in other populations of D. serrata (Delcourt et al 2012), in red deer (Kruuk et al 2000), and in North American red squirrels (McFarlane et al 2014); however, we cannot exclude the possibility that V A exists here for fitness but we lacked the power to detect it. We were able to detect statistically significant variance of a magnitude smaller than 0.008 for the eigenvectors of the wing-shape additive covariance matrix; however, we had reduced power to detect additive genetic variance in fitness for two reasons.…”

“…Contrary to predictions, this trait combination actually had a higher V A estimate of 0.31, compared to V D of 0.16, given by the projections of this vector, standardized to unit length, through the additive and dominance covariance matrices, respectively. This vector of selection differentials is unbiased by environmentally induced covariances between traits and fitness (Robertson 1966;Lynch and Walsh 1998;Delcourt et al 2012); however, predicted evolutionary responses characterized by s g do not distinguish between the effect of selection acting directly on the traits of interest and selection acting through correlated traits (Stinchcombe et al 2013). Although s g is under directional selection, the combination of positive and negative trait loadings contained in this vector indicate that additive genetic variance may be maintained by antagonistic selection on the individual traits comprising this multivariate trait combination.…”

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

“…Under the pure pleiotropy class of model, observed mutational heritability on the order of 0.001 implies that standardized stabilizing selection gradients on traits must be 20.001 (V s = 500) or weaker to maintain any level of heritability (Johnson and Barton 2005, equation A25). While this strength of stabilizing selection has been observed on the genetic variance of some individual CHC traits, it varies considerably among traits and has been reported to be up to 100 times stronger on one CHC expressed in males of our study species (Delcourt et al 2012). A pure pleiotropy model of mutation-selection balance is Figure 5 The observed (solid black circles) relationship between mutational (x-axis) and additive genetic (y-axis) heritability and the fit of the neutral drift (dashed black line), Gaussian approximation (gray) and house-of-cards (black) models.…”

“…D. serrata CHCs, waxy lipids present on the cuticle, are under directional sexual selection through mate choice but also have consequences for nonsexual fitness (Higgie and Blows 2007;Chenoweth et al 2010;Hine et al 2011;McGuigan et al 2011;Delcourt et al 2012). CHC profiles of individual males were determined using standard gas chromatography (GC) protocols (Sztepanacz and Rundle 2012).…”