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

Abstract

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.

Keywords: diploid selection; host-parasite co-evolution; matching-phenotype interaction; recombination plasticity; modifier model.

Figure 1

The effect of recombination rate in the parasite ( $$r^{\mathrm{p}}$$ ) on the estimation of the optimal constant recombination rate in the host ( $$r_{\mathrm{opt}}^{\mathrm{h}}$$ ). The colored curves show the lower (blue) and the upper (red) estimates. All simulations are conducted for the case of obligate parasitism (=1).

Figure 2

The evolutionary advantage of plastic recombination over non-zero optimal constant recombination, under in-phase (a) and anti-phase (b) dominance. The colored markers show regimes where the prevention (yellow) and the remediation (red) strategies are favored, either totally (circles) or partially (triangles).

Figure 3

The system’s dynamics under different regimes favoring plastic recombination. The plots show the last 500 out of 10,000 generations of the competition between the optimal constant recombination and plastic recombination; yet, the pattern is qualitatively similar also for other time windows. The colored curves stand for the host (green) and the parasite (orange). A, B and M denote, respectively, the two interaction-mediating loci and the modifier locus while W denotes the population’s mean fitness. All examples stand for anti-phase dominance and prevention strategy: (a) A regime with strong overall selection: $$s^{\mathrm{h}}\approx 0.88$$ , $$s^{\mathrm{p}}\approx 0.91$$ . The optimal constant recombination in the host is high: $$r_{\mathrm{opt}}^{\mathrm{h}}\approx 0.25.$$ The oscillations are fairly regular. The modifier allele for plastic recombination generally increases in frequency, again with fairly regular oscillations; (b) A regime with extremely strong overall selection: $$s^{\mathrm{h}}\approx 0.98$$ , $$s^{\mathrm{p}}>0.99$$ . The optimal constant recombination in the host is high: $$r_{\mathrm{opt}}^{\mathrm{h}}=0.32.$$ The oscillations are regular. The modifier allele for plastic recombination generally increases in frequency, again with fairly regular oscillations; (c) A regime with weak overall selection due to weak selection in the host: $$s^{\mathrm{h}}\approx 0.14$$ , $$s^{\mathrm{p}}\approx 0.70$$ . The optimal constant recombination in the host is very low: $$r_{\mathrm{opt}}^{\mathrm{h}}<0.01.$$ The oscillations are irregular. Although the modifier allele for plastic recombination generally increases in frequency, its oscillations are substantially irregular; (d) A regime with weak overall selection due to weak selection in the parasite: $$s^{\mathrm{h}}\approx 0.85$$ , $$s^{\mathrm{p}}\approx 0.16$$ . The optimal constant recombination in the host is very low: $$r_{\mathrm{opt}}^{\mathrm{h}}<0.01.$$ The oscillations are irregular. Although the modifier allele for plastic recombination generally increases in frequency, its dynamics are considerably irregular; in certain time windows (like here), the decline of the modifier allele for plastic recombination may even temporally prevail.

Figure 3

The system’s dynamics under different regimes favoring plastic recombination. The plots show the last 500 out of 10,000 generations of the competition between the optimal constant recombination and plastic recombination; yet, the pattern is qualitatively similar also for other time windows. The colored curves stand for the host (green) and the parasite (orange). A, B and M denote, respectively, the two interaction-mediating loci and the modifier locus while W denotes the population’s mean fitness. All examples stand for anti-phase dominance and prevention strategy: (a) A regime with strong overall selection: $$s^{\mathrm{h}}\approx 0.88$$ , $$s^{\mathrm{p}}\approx 0.91$$ . The optimal constant recombination in the host is high: $$r_{\mathrm{opt}}^{\mathrm{h}}\approx 0.25.$$ The oscillations are fairly regular. The modifier allele for plastic recombination generally increases in frequency, again with fairly regular oscillations; (b) A regime with extremely strong overall selection: $$s^{\mathrm{h}}\approx 0.98$$ , $$s^{\mathrm{p}}>0.99$$ . The optimal constant recombination in the host is high: $$r_{\mathrm{opt}}^{\mathrm{h}}=0.32.$$ The oscillations are regular. The modifier allele for plastic recombination generally increases in frequency, again with fairly regular oscillations; (c) A regime with weak overall selection due to weak selection in the host: $$s^{\mathrm{h}}\approx 0.14$$ , $$s^{\mathrm{p}}\approx 0.70$$ . The optimal constant recombination in the host is very low: $$r_{\mathrm{opt}}^{\mathrm{h}}<0.01.$$ The oscillations are irregular. Although the modifier allele for plastic recombination generally increases in frequency, its oscillations are substantially irregular; (d) A regime with weak overall selection due to weak selection in the parasite: $$s^{\mathrm{h}}\approx 0.85$$ , $$s^{\mathrm{p}}\approx 0.16$$ . The optimal constant recombination in the host is very low: $$r_{\mathrm{opt}}^{\mathrm{h}}<0.01.$$ The oscillations are irregular. Although the modifier allele for plastic recombination generally increases in frequency, its dynamics are considerably irregular; in certain time windows (like here), the decline of the modifier allele for plastic recombination may even temporally prevail.

Figure 4

The evolutionary advantage of plastic recombination over zero optimal constant recombination, under in-phase (a) and anti-phase (b) dominance. The colored markers show regimes where the prevention (yellow) and the remediation (red) strategies are favored, either totally (circles) or partially (triangles).

Figure 5

The effect of the magnitude of recombination plasticity on the proportion of regimes favoring plastic recombination. The line styles stand for in-phase (sold) and anti-phase (dashed) dominance, while the marker colors stand for prevention (yellow) and remediation (red) strategies.