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"Resistance Is Futile": Weaker Selection for Resistance by Abundant Parasites Increases Prevalence and Depresses Host Density.

Authors
  • Walsman, Jason C
  • Duffy, Meghan A
  • Cáceres, Carla E
  • Hall, Spencer R
Type
Published Article
Journal
The American Naturalist
Publisher
The University of Chicago Press
Publication Date
Jun 01, 2023
Volume
201
Issue
6
Pages
864–879
Identifiers
DOI: 10.1086/724426
PMID: 37229705
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

AbstractTheory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a "resistance is futile" outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts' resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, "transmission rate") along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations.

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