‘Resistance is futile’: Weaker selection for resistance during larger epidemics further increases prevalence and depresses host density

Abstract

What determines how much resistance hosts evolve? One might intuit that hosts evolve higher resistance when parasites are more abundant. However, the opposite pattern can arise due to costs of resistance. Here we illustrate with mathematical, experimental, and field approaches how ecological context can increase parasite abundance and select for lower resistance. "Resistance is futile" when all host genotypes become sufficiently infected. To make this argument, we first analyzed an eco-evolutionary model of parasites, hosts, and resources of hosts. We determined eco-evolutionary outcomes for resistance (mathematically, transmission rate) and densities along gradients that drive epidemic size. When epidemic drivers are high, hosts evolve lower resistance, amplifying epidemics and decreasing host density. Experimental mesocosms qualitatively agreed. In the experiment, higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites. Evolving zooplankton hosts were less resistant at high nutrients than at low. Less resistance, in turn, was associated with higher infection prevalence and lower host density. We also analyzed the size of naturally occurring epidemics, finding a broad, bimodal distribution of epidemic sizes consistent with the eco-evolutionary model. Together, our three approaches supported predictions that high epidemic drivers lead to evolution of lower resistance which drives higher prevalence and lower host density.

Predation shifts coevolution toward higher host contact rate and parasite virulence

“…With host evolution (figure 2 e–h ), hosts evolve increasing contact rate in response to increasing predation. The increasing contact rate increases prevalence and can eventually lead to ‘resistance is futile’ [40] (i.e. behavioural resistance through a decreased contact rate) and hosts evolve a maximum contact rate to minimize predation risk (blue curve in figure 2 e ; see electronic supplementary material, figure S2 for more detail).…”

The evolution of age-specific resistance to infectious disease

“…For sufficiently high values of 𝛽 0 , the outcome depends on whether the host population remains viable (see Supplementary Materials), in which case resistance may tend towards either a high value if the pathogen is sufficiently virulent (Fig. 4A) or else a low value if disease prevalence approaches 100% with most individuals infected very shortly after birth (with selection against ineffective resistance, as observed in some empirical systems [57]; Fig. 4B).…”

The evolution of age-specific resistance to infectious disease

“…In evolutionary terms, this also causes both juvenile and adult resistance to rise (figure 4), with similar differences between trade-offs as described above (electronic supplementary material, figures S2 and S3). For sufficiently high values of β 0 , the outcome depends on whether the host population remains viable (see the electronic supplementary material), in which case resistance may tend towards either a high value if the pathogen is sufficiently virulent (figure 4a) or else a low value if disease prevalence approaches 100% with most individuals infected very shortly after birth (with selection against ineffective resistance, as observed in some empirical systems [57]; figure 4b).…”