Coinfecting parasites can modify fluctuating selection dynamics in host-parasite coevolution

Abstract

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host-parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.

Keywords: Red Queen dynamics; coevolution; coinfection; resource competition; virulence.

FIGURE 1

(a) Mean infection prevalence, (b) mean host population density, (c) variance in host population density across generations, and (d) mean change in host clone frequencies over time (i.e., fluctuating selection dynamics; range: 0–1) examined across different levels of parasite fecundity and fitness costs of infection to the hosts during the last 100 generations of the phase one of the simulation (coinfecting genetically nonspecific parasite not present). After Lively (2010b), the reproductive output of uninfected hosts (b _U), the probabilities for uninfected and infected hosts to enter the population (same for all clones) were chosen to be 20, 0.10, and 0.02, respectively. Numbers 1–4 in the first panel refer to combinations of parameter values for which examples of dynamics of host clone frequencies in individual runs of the simulation are presented in Figure 2

FIGURE 2

Examples of the dynamics of host clone frequencies (nine clones) in individual runs of the simulation representing regions of parameter space with different epidemiological and/or coevolutionary dynamics (numbers 1–4 in Figure 1a). (a) Parasite‐induced fitness costs to the hosts (C _A) and parasite fecundity (β _A) are 0.5 and 5, respectively (region 1 in Figure 1a), (b) C _A and β _A are 0.5 and 20, respectively (region 2 in Figure 1a), (c) C _A and β _A are 0.8 and 20, respectively (region 3 in Figure 1a), (d) C _A and β _A are 0.9 and 20, respectively (region 4 in Figure 1a)

FIGURE 3

The relationship between the number of infected host individuals of one host clone in generation t and the probability of the individuals of the same clone to become infected in generation t + 1 during the last 100 generations of one simulation run. (a) Parasite‐induced fitness costs to the hosts (C _A) and parasite fecundity (β _A) are 0.78 and 20, respectively. (b) C _A is 0.775 and β _A is 20. (c) C _A is 0.77 and β _A is 20. These examples are chosen to demonstrate the abrupt change from the fluctuating selection dynamics to stable infection dynamics when fitness costs of infection to the hosts decrease

FIGURE 4

Mean change in host clone frequencies over time (i.e., fluctuating selection dynamics; range: 0–1) across different levels of fecundity and fitness costs induced to the hosts by the genetically specific parasite species A during the last 100 generations of the phase two of the simulation when the coinfecting genetically nonspecific parasite species B that uses different host resources was present in the host population. Coinfection leads to a multiplicative increase in fitness costs to the hosts. Plots a‐t show the results for different levels of parasite B fecundity and fitness costs it induces to the hosts. After Lively (2010b), the reproductive output of uninfected hosts (b _U), the probabilities for uninfected and infected hosts to enter the population (both parasite species, same for all clones) were chosen to be 20, 0.10, and 0.02, respectively

FIGURE 5

Mean change in host clone frequencies over time (i.e., fluctuating selection dynamics; range: 0–1) across different levels of fecundity and fitness costs induced to the hosts by the genetically specific parasite species A during the last 100 generations of the phase two of the simulation when the coinfecting genetically nonspecific parasite species B that uses the same host resources was present in the host population. Coinfection leads to competition for the shared host resources and thus reduces parasite fecundity. Plots a–t show the results for different levels of parasite B fecundity and fitness costs it induces to the hosts. After Lively (2010b), the reproductive output of uninfected hosts (b _U), the probabilities for uninfected and infected hosts to enter the population (both parasite species, same for all clones) were chosen to be 20, 0.10, and 0.02, respectively