Host resources and parasite traits interact to determine the optimal
combination of host parasite-mitigation strategies
Abstract
1. Organisms have evolved diverse strategies to manage parasite
infections. Broadly, hosts may avoid infection by altering behaviour,
resist infection by targeting parasites, or tolerate infection by
repairing associated damage. Effectiveness of a strategy depends on
interactions between, e.g., resource availability, parasite traits
(virulence, life-history) and the host itself (nutritional status,
immunopathology). 2. To understand how these factors shape host
parasite-mitigation strategies, we developed a mathematical model of
within-host, parasite-immune dynamics in the context of helminth
infections. The model incorporated host nutrition and resource
allocation to different mechanisms of immune response: larval parasite
prevention; adult parasite clearance; damage repair (tolerance). We also
considered a non-immune strategy: avoidance via anorexia, reducing
intake of infective stages. Resources not allocated to immune processes
promoted host condition, whereas harm due to parasites and
immunopathology diminished it. Maximising condition (a proxy for
fitness), we determined optimal host investment for each
parasite-mitigation strategy, singly and combined, across different
environmental resource levels and parasite trait values. 3. Which
strategy was optimal varied with scenario. Tolerance generally performed
well, especially with high resources. Success of the different
resistance strategies (larval prevention or adult clearance) tracked
relative virulence of larval and adult parasites: slowly maturing,
highly damaging larvae favoured prevention; rapidly maturing, less
harmful larvae favoured clearance. Anorexia was viable only in the
short-term, due to reduced host nutrition. Combined strategies always
outperformed any lone strategy: these were dominated by tolerance, with
some investment in resistance. 4. Choice of parasite mitigation strategy
has profound consequences for hosts, impacting their condition, survival
and reproductive success. We show the efficacy of different strategies
is highly dependent on timescale, parasite traits and resource
availability. Models that integrate such factors can inform the
collection and interpretation of empirical data, to understand how those
drivers interact to shape host immune responses in natural systems.