An evolutionary quantitative genetics model for phenotypic (co)variances under limited dispersal, with an application to socially synergistic traits

Abstract

Darwinian evolution consists of the gradual transformation of heritable traits due to natural selection and the input of random variation by mutation. Here, we use a quantitative genetics approach to investigate the coevolution of multiple quantitative traits under selection, mutation, and limited dispersal. We track the dynamics of trait means and of variance–covariances between traits that experience frequency‐dependent selection. Assuming a multivariate‐normal trait distribution, we recover classical dynamics of quantitative genetics, as well as stability and evolutionary branching conditions of invasion analyses, except that due to limited dispersal, selection depends on indirect fitness effects and relatedness. In particular, correlational selection that associates different traits within‐individuals depends on the fitness effects of such associations between‐individuals. We find that these kin selection effects can be as relevant as pleiotropy for the evolution of correlation between traits. We illustrate this with an example of the coevolution of two social traits whose association within‐individuals is costly but synergistically beneficial between‐individuals. As dispersal becomes limited and relatedness increases, associations between‐traits between‐individuals become increasingly targeted by correlational selection. Consequently, the trait distribution goes from being bimodal with a negative correlation under panmixia to unimodal with a positive correlation under limited dispersal.

How does the strength of selection influence genetic correlations?

“…In terms of selection, we considered a fitness peak with an optimum, in line with most theory on the topic, but genetic correlations can also be favored by other forms of selection, notably disruptive selection (Bolstad et al. 2015), or negative frequency dependence caused by individual interactions (Mullon and Lehmann 2019), which may lead to different dependencies of genetic correlations on the strength of selection and genetic drift.…”

“…An interesting extension may be to allow for modular mutation effects, or restricted pleiotropy, whereby each locus can only modify a subset of traits by mutations (Chevin et al 2010;Chebib and Guillaume 2017), to investigate whether the mutation regime has a stronger effect on mutation correlations in these scenarios. In terms of selection, we considered a fitness peak with an optimum, in line with most theory on the topic, but genetic correlations can also be favored by other forms of selection, notably disruptive selection (Bolstad et al 2015), or negative frequency dependence caused by individual interactions (Mullon and Lehmann 2019), which may lead to different dependencies of genetic correlations on the strength of selection and genetic drift.…”

How does the strength of selection influence genetic correlations ?

“…An interesting extension may be to allow for modular mutation effects, or restricted pleiotropy, whereby each locus can only modify a subset of traits by mutations (Chebib and Guillaume, 2017;Chevin et al, 2010), to investigate whether the mutation regime has a stronger effect on mutation correlations in these scenarios. In terms of selection, we considered a fitness peak with an optimum, in line with most theory on the topic, but genetic correlations can also be favored by other forms of selection, notably disruptive selection (Bolstad et al, 2015), or negative frequency dependence caused by individual interactions (Mullon and Lehmann, 2019), which may lead to different dependencies of genetic correlations on the strength of selection and genetic drift.…”

Evolution of division of labour in mutualistic symbiosis

“…Here, we theoretically explored the evolutionary dynamics describing the development of division of labour in mutualistic symbiosis and revealed when organisms evolve to specialize in and rely exclusively on symbiotic interaction. Since the evolution of division of labour has been studied in the context of the evolution of multicellularity and sociality [3,[17][18][19][20], the cost of failing to find partners has not received much attention (but see [3]), which will be shown in this paper to play a pivotal role in environmentally acquired symbiosis. Implication to the evolution of generalists versus specialists with dispersal in heterogeneous environment will be discussed later.…”