Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration

Abstract

Parasites have long been thought to influence the evolution of migration, but precisely determining the conditions under which this occurs by quantifying costs of infection remains a challenge. Here we developed a model that demonstrates how the metric used to describe infection (richness/diversity, prevalence or intensity) shapes the prediction of whether migration will evolve. The model shows that predictions based on minimizing richness yield opposite results compared to those based on minimizing prevalence, with migration only selected for when minimizing prevalence. Consistent with these findings, empirical studies that measure parasite diversity typically find that migrants are worse off than residents, while those measuring prevalence or intensity find the opposite. Our own empirical analysis of fish parasite data finds that migrants (of all types) have higher parasite richness than residents, but with no significant difference in either prevalence or intensity.

Keywords: comparative analysis; disease ecology; evolutionarily stable strategy; host–parasite interaction; mathematical model; movement ecology.

Figure 1.

Model schematic. A fraction (1 − θ) of individuals stay in environment 1 year-round (where they are infected by parasite 1 at rate β₁), the remaining individuals migrate to environment 2 for part of the year (where they are infected by parasite 2 at rate β₂) but return to environment 1 to reproduce.

Figure 2.

Difference in infection prevalence of residents (p_R) and migrants (p_M). Shown are cases where migrants have lower infection prevalence, residents have lower infection prevalence, and where migrants go extinct. Parameter values: β₁ = 1, β₂ = 1 (a) or 0 ≤ β₂ ≤ 2 (b,c); φ₁ = 1, φ₂ = 1 (b) or 0 ≤ φ₂ ≤ 3 (a,c); σ_1R = 0.5, σ_2R = 0.5 (c) or 0 ≤ σ_2R ≤ σ_SR (a,b), all other values are given in table S1 in [38]. The survival and fecundity of an individual with both parasites are the minimum survival and fecundity of having either one of the parasites.

Figure 3.

Evolutionarily stable probability of migration as a result of trade-offs between fecundity, survival and transmission rates. Parameter values are the same as figure 2 and lines from figure 2 are shown for comparison. Black points indicate a strategy of always migrating (θ_ESS = 1), grey points indicate never migrating (θ_ESS = 0) and intermediate values of θ_ESS were never observed.