A Numerical Model Supports the Evolutionary Advantage of Recombination Plasticity in Shifting Environments.

AbstractNumerous empirical studies have witnessed an increase in meiotic recombination rate in response to physiological stress imposed by unfavorable environmental conditions. Thus, inherited plasticity in recombination rate is hypothesized to be evolutionarily advantageous in changing environments. Previous theoretical models proceeded from the assumption that organisms increase their recombination rate when the environment becomes more stressful and demonstrated the evolutionary advantage of such a form of plasticity. Here, we numerically explore a complementary scenario-when the plastic increase in recombination rate is triggered by the environmental shifts. Specifically, we assume increased recombination in individuals developing in a different environment than their parents and, optionally, also in offspring of such individuals. We show that such shift-inducible recombination is always superior when the optimal constant recombination implies an intermediate rate. Moreover, under certain conditions, plastic recombination may also appear beneficial when the optimal constant recombination is either zero or free. The advantage of plastic recombination was better predicted by the range of the population's mean fitness over the period of environmental fluctuations, compared with the geometric mean fitness. These results hold for both panmixia and partial selfing, with faster dynamics of recombination modifier alleles under selfing. We think that recombination plasticity can be acquired under the control of environmentally responsive mechanisms, such as chromatin epigenetics remodeling.

Modeling the evolution of recombination plasticity: A prospective review.

Meiotic recombination is one of the main sources of genetic variation, a fundamental factor in the evolutionary adaptation of sexual eukaryotes. Yet, the role of variation in recombination rate and other recombination features remains underexplored. In this review, we focus on the sensitivity of recombination rates to different extrinsic and intrinsic factors. We briefly present the empirical evidence for recombination plasticity in response to environmental perturbations and/or poor genetic background and discuss theoretical models developed to explain how such plasticity could have evolved and how it can affect important population characteristics. We highlight a gap between the evidence, which comes mostly from experiments with diploids, and theory, which typically assumes haploid selection. Finally, we formulate open questions whose solving would help to outline conditions favoring recombination plasticity. This will contribute to answering the long-standing question of why sexual recombination exists despite its costs, since plastic recombination may be evolutionary advantageous even in selection regimes rejecting any non-zero constant recombination.

Erratum: Rybnikov et al. Selection for Plastic, Pathogen-Inducible Recombination in a Red Queen Model with Diploid Antagonists. Pathogens 2021, 10, 898.

In the original article, there was a mistake published in Figure 3 [...].

Selection for Plastic, Pathogen-Inducible Recombination in a Red Queen Model with Diploid Antagonists.

Antagonistic interactions and co-evolution between a host and its parasite are known to cause oscillations in the population genetic structure of both species (Red Queen dynamics). Potentially, such oscillations may select for increased sex and recombination in the host, although theoretical models suggest that this happens under rather restricted values of selection intensity, epistasis, and other parameters. Here, we explore a model in which the diploid parasite succeeds to infect the diploid host only if their phenotypes at the interaction-mediating loci match. Whenever regular oscillations emerge in this system, we test whether plastic, pathogen-inducible recombination in the host can be favored over the optimal constant recombination. Two forms of the host recombination dependence on the parasite pressure were considered: either proportionally to the risk of infection (prevention strategy) or upon the fact of infection (remediation strategy). We show that both forms of plastic recombination can be favored, although relatively infrequently (up to 11% of all regimes with regular oscillations, and up to 20% of regimes with obligate parasitism). This happens under either strong overall selection and high recombination rate in the host, or weak overall selection and low recombination rate in the host. In the latter case, the system's dynamics are considerably more complex. The prevention strategy is favored more often than the remediation one. It is noteworthy that plastic recombination can be favored even when any constant recombination is rejected, making plasticity an evolutionary mechanism for the rescue of host recombination.

Fitness dependence preserves selection for recombination across diverse mixed mating strategies.

Meiotic recombination and the factors affecting its rate and fate in nature have inspired many studies in theoretical evolutionary biology. Classical theoretical models have inferred that recombination can be favored under a rather restricted parameter range. Thus, the ubiquity of recombination in nature remains an open question. However, these models assumed constant recombination with an equal rate across all individuals within the population, whereas empirical evidence suggests that recombination may display certain sensitivity to ecological stressors and/or genotype fitness. Models assuming condition-dependent recombination show that such a strategy can often be favored over constant recombination. Moreover, in our recent model with panmictic populations subjected to purifying selection, fitness-dependent recombination was quite often favored even when any constant recombination was rejected. By using numerical modeling, we test whether such a 'recombination-rescuing potential' of fitness dependence holds also beyond panmixia, given the recognized effect of mating strategy on the evolution of recombination. We show that deviations from panmixia generally increase the recombination-rescuing potential of fitness dependence, with the strongest effect under intermediate selfing or high clonality. We find that under partial clonality, the evolutionary advantage of fitness-dependent recombination is determined mostly by selection against heterozygotes and additive-by-additive epistasis, while under partial selfing, additive-by-dominance epistasis is also a driver.

Seasonal changes in recombination characteristics in a natural population of Drosophila melanogaster.

Environmental seasonality is a potent evolutionary force, capable of maintaining polymorphism, promoting phenotypic plasticity and causing bet-hedging. In Drosophila, environmental seasonality has been reported to affect life-history traits, tolerance to abiotic stressors and immunity. Oscillations in frequencies of alleles underlying fitness-related traits were also documented alongside SNPs across the genome. Here, we test for seasonal changes in two recombination characteristics, crossover rate and crossover interference, in a natural D. melanogaster population from India using morphological markers of the three major chromosomes. We show that winter flies, collected after the dry season, have significantly higher desiccation tolerance than their autumn counterparts. This difference proved to hold also for hybrids with three independent marker stocks, suggesting its genetic rather than plastic nature. Significant between-season changes are documented for crossover rate (in 9 of 13 studied intervals) and crossover interference (in four of eight studied pairs of intervals); both single and double crossovers were usually more frequent in the winter cohort. The winter flies also display weaker plasticity of both recombination characteristics to desiccation. We ascribe the observed differences to indirect selection on recombination caused by directional selection on desiccation tolerance. Our findings suggest that changes in recombination characteristics can arise even after a short period of seasonal adaptation (~8-10 generations).

The evolutionary advantage of fitness-dependent recombination in diploids: A deterministic mutation-selection balance model.

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.

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

Meiotic recombination is evolutionarily ambiguous, as being associated with both benefits and costs to its bearers, with the resultant dependent on a variety of conditions. While existing theoretical models explain the emergence and maintenance of recombination, some of its essential features remain underexplored. Here we focus on one such feature, recombination plasticity, and test whether recombination response to stress is fitness-dependent. We compare desiccation stress effects on recombination rate and crossover interference in chromosome 3 between desiccation-sensitive and desiccation-tolerant Drosophila lines. We show that relative to desiccation-tolerant genotypes, desiccation-sensitive genotypes exhibit a significant segment-specific increase in single- and double-crossover frequencies across the pericentromeric region of chromosome 3. Significant changes (relaxation) in crossover interference were found for the interval pairs flanking the centromere and extending to the left arm of the chromosome. These results indicate that desiccation is a recombinogenic factor and that desiccation-induced changes in both recombination rate and crossover interference are fitness-dependent, with a tendency of less fitted individuals to produce more variable progeny. Such dependence may play an important role in the regulation of genetic variation in populations experiencing environmental challenges.

What drives the evolution of condition-dependent recombination in diploids? Some insights from simulation modelling.

While the evolutionary advantages of non-zero recombination rates have prompted diverse theoretical explanations, the evolution of essential recombination features remains underexplored. We focused on one such feature, the condition dependence of recombination, viewed as the variation in within-generation sensitivity of recombination to external (environment) and/or internal (genotype) conditions. Limited empirical evidence for its existence comes mainly from diploids, whereas theoretical models show that it only easily evolves in haploids. The evolution of condition-dependent recombination can be explained by its advantage for the selected system (indirect effect), or by benefits to modifier alleles, ensuring this strategy regardless of effects on the selected system (direct effect). We considered infinite panmictic populations of diploids exposed to a cyclical two-state environment. Each organism had three selected loci. Examining allele dynamics at a fourth, selectively neutral recombination modifier locus, we frequently observed that a modifier allele conferring condition-dependent recombination between the selected loci displaced the allele conferring the optimal constant recombination rate. Our simulations also confirm the results of theoretical studies showing that condition-dependent recombination cannot evolve in diploids on the basis of direct fitness-dependent effects alone. Therefore, the evolution of condition-dependent recombination in diploids can be driven by indirect effects alone, i.e. by modifier effects on the selected system.This article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.