How does the strength of selection influence genetic correlations?

Abstract

Genetic correlations between traits can strongly impact evolutionary responses to selection, and may thus impose constraints on adaptation. Theoretical and empirical work has made it clear that without strong linkage and with random mating, genetic correlations at evolutionary equilibrium result from an interplay of correlated pleiotropic effects of mutations, and correlational selection favoring combinations of trait values. However, it is not entirely clear how change in the overall strength of stabilizing selection across traits (breadth of the fitness peak, given its shape) influences this compromise between mutation and selection effects on genetic correlation. Here, we show that the answer to this question crucially depends on the intensity of genetic drift. In large, effectively infinite populations, genetic correlations are unaffected by the strength of selection, regardless of whether the genetic architecture involves common small-effect mutations (Gaussian regime), or rare large-effect mutations (House-of-Cards regime). In contrast in finite populations, the strength of selection does affect genetic correlations, by shifting the balance from drift-dominated to selection-dominated evolutionary dynamics. The transition between these domains depends on mutation parameters to some extent, but with a similar dependence of genetic correlation on the strength of selection. Our results are particularly relevant for understanding how senescence shapes patterns of genetic correlations across ages, and genetic constraints on adaptation during colonization of novel habitats.

Pleiotropy or linkage? Their relative contributions to the genetic correlation of quantitative traits and detection by multitrait GWA studies

“…Nevertheless, covariance should principally build-up from linkage disequilibria within pairs, caused by correlational selection on the two traits. Note that the pleiotropic case is fully covered in Lande (1980 , 1984 ); Zhang and Hill (2003) ; Chantepie and Chevin (2020) .…”

“…Correlational selection is when selection favors correlated values at phenotypic traits, which should translate into correlated genetic effects at the underlying loci affecting the traits. This has been shown to be the case in models attempting to approximate the level of genetic variance and covariance maintained at mutation-selection balance at pleiotropic loci affecting polygenic traits ( Lande 1980 ; Turelli 1985 ; Zhang and Hill 2003 ; Chantepie and Chevin 2020 ). For the case of tight linkage between pairs of loci affecting separate traits, Lande (1984) suggested that it “is nearly equivalent to” pleiotropic loci affecting both traits.…”

“…However, the conditions under which this statement is correct have not been fully elucidated. Yet, the fact that the same equilibrium genetic correlation under correlational selection has been obtained under different theoretical assumptions about the rate and effect size of mutations by Lande (1984) and Zhang and Hill (2003) tends to suggest that Lande’s statement may hold generally (see also Chantepie and Chevin 2020 , for a recent reanalysis).…”

“…, there is no mutational correlation ( ). Chantepie and Chevin (2020) recently showed that the equivalence between the Gaussian and house-of-cards regimes holds even when . They further derived the equilibrium G-matrix under the Gaussian regime at mutation–selection–drift balance, which will be useful in this study for generating expectations under Gaussian assumptions.…”

“…Additionally, levels of trait genetic covariation can be influenced by other evolutionary processes that affect allele frequencies, and the covariation of allelic values in a population [ e.g. , migration ( Guillaume and Whitlock 2007 ), drift ( Griswold et al 2007 ; Chantepie and Chevin 2020 ), inbreeding ( Lande 1984 ), and phenotypic plasticity ( Draghi and Whitlock 2012 )]. Migration affects genetic covariation because when it is sufficiently high (relative to selection in the focal population), then combinations of alleles coming from a source population will also be maintained in the focal population.…”