Fitness-Dependent Recombination Can Be Evolutionarily Advantageous in Diploids: a Deterministic Mutation–Selection–Balance Model

Abstract

Recombination's omnipresence in nature is one of the most intriguing problems in evolutionary biology. The question of why recombination exhibits certain general features is no less interesting than that of why it exists at all. One such feature is recombination's fitness dependence (FD). The so far developed population-genetics models have focused on the evolution of FD recombination mainly in haploids, although the empirical evidence for this phenomenon comes mostly from diploids. Using numerical analysis of modifier models for infinite panmictic populations, we show here that FD recombination can be evolutionarily advantageous in diploids subjected to purifying selection. This advantage is associated with benefits from the differential rate of disruption of lower-vs higher-fitness genotypes, that can be manifested in systems with at least three selected loci. We also show that in systems with linked modifier, an additional contribution to the evolutionary advantage of FD recombination may come from fitness-dependence of the intensity of modifier linkage to the selected system, although the contribution of the last effect vanishes with tighter linkage within the selected system. We also show that in systems with three selected loci, FD recombination may give rise to negative crossover interference, which may be beneficial by itself. Yet, the role of such FD-induced crossover interference in the evolutionary advantage of FD recombination is minor. Remarkably, FD recombination was often favored in situations where any constant non-zero recombination was rejected, implying a relaxation of the rather strict constraints on major parameters (e.g., selection intensity and epistasis) required for the evolutionary advantage of non-zero recombination formulated by classical models.

The evolutionary advantage of condition-dependent recombination in a Red Queen model with diploid antagonists

“…At that, both the benefits and the costs are function of amplitude of RR plasticity. The interplay between these two function is not trivial, and the net function can be even nonmonotonous, so that an intermediate amplitude of RR plasticity sometimes appears optimal, as in our previous study [62]. The examined forms of CD recombination appeared to be favored over the corresponding optimal constant RR in different proportion of cases.…”

“…We considered three forms of CD recombination: (i) parasite-dependent ID recombination were examined in the models with two and three selected loci, while FD recombination -only in the model with three selected loci. The reason is that FD recombination is imaginable only in the presence of variation in fitness among those genotypes in which recombination has fitness consequences in the next generation, which requires at least three selected loci [60,62].…”

“…The empirical evidence for CD recombination comes mostly from diploids. At the same time, theoretical diploid-selection models confirmed the evolutionary advantage of ED recombination [59,60], but obtained less clear results for FD recombination [60][61][62]. These theoretical studies considered cyclical selection and mutation-selection balance.…”

Desiccation-induced changes in recombination rate and crossover interference in Drosophila melanogaster: evidence for fitness-dependent plasticity

“…In diploids, the "abandon-ship" mechanism has been shown to be inefficient (Agrawal et al 2005). However, our recent simulations demonstrate that fitness-dependent recombination can evolve in diploids under certain scenarios, such as cyclical selection (Rybnikov et al 2017), Red Queen dynamics (Rybnikov et al 2018a), and mutation-selection balance (Rybnikov et al 2018b). In all our models, fitness-dependence was assumed only for recombination within the selected system.…”

“…This can make plastic recombination beneficial only if there is a variation in fitness among heterozygous genotypes, which requires at least three selected loci. Importantly, the evolutionary advantage/disadvantage of fitness-dependent recombination is determined by a trade-off between two opposite effects: benefits from protecting best allele combinations, and costs of shifting population mean recombination rate (Rybnikov et al 2018b). The cost often outbalances the benefits, which may be one of the reasons why some experimental-evolution studies reported no selection for recombination rate plasticity (Kerstes et al 2012;Kohl and Singh 2018).…”