The evolutionary advantage of fitness-dependent recombination 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. We ascribe this advantage to the differential rate of disruption of lower- versus higher-fitness genotypes, which can be manifested in selected systems with at least three loci. We also show that if the modifier is linked to such selected system, it can additionally benefit from modifying this linkage in a fitness-dependent manner. The revealed evolutionary advantage of FD recombination appeared robust to crossover interference within the selected system, either positive or negative. Remarkably, FD recombination was often favored in situations where any constant nonzero recombination was evolutionarily disfavored, implying a relaxation of the rather strict constraints on major parameters (e.g., selection intensity and epistasis) required for the evolutionary advantage of nonzero recombination formulated by classical models.

Keywords: diploids; fitness dependence; purifying selection; recombination; recombination modifier.

Figure 1

The evolutionary advantage of FD recombination over zero optimal constant RR: the effect of key selection parameters. The data stand for the system with three selected loci and no crossover interference within the selected system (though the pattern appeared to be strongly robust to crossover interference). In each heat map, x and y axes stand, respectively, for the deleterious effect of mutations (s) and the absolute value of negative additive‐by‐additive epistasis (|e _a×a|). The colors stand for the proportion of cases where FD recombination is favored (as a ratio to the total number of cases with the given parameter combination). No color means that no cases with zero optimal constant RR were observed under the given parameter combination

Figure 2

The evolutionary advantage of FD recombination over intermediate optimal constant RR: the effect of key selection parameters and crossover interference within the selected system. The data stand for the system with three selected loci and linked modifier, +FD‐strategy. In each heat map, x and y axes stand, respectively, for the deleterious effect of mutations (s) and the absolute value of negative additive‐by‐additive epistasis (|e _a×a|). The colors stand for the proportion of cases where FD recombination is favored (as a ratio to the total number of cases with the given parameter combination). No color means that no cases with intermediate optimal constant RR were observed under the given parameter combination

Figure 3

The effect of FD‐induced modulation of modifier linkage on the evolutionary advantage of FD recombination over intermediate optimal constant RR. The data stand for the system with three selected loci and linked modifier, +FD‐strategy. The “distant‐interval” +FD‐strategy can still be favored, although it is less advantageous than the “two‐interval” +FD‐strategy. This suggests that FD‐induced modulation of modifier linkage may play a certain role in systems with linked modifier, decreasing with linkage intensity between the selected loci