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Host resources and parasite traits interact to determine the optimal combination of host parasite-mitigation strategies
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  • Andrew Dean,
  • Dylan Childs,
  • Yolanda Corripio-Miyar,
  • Mike Evans,
  • Adam Hayward,
  • Fiona Kenyon,
  • Luke McNally,
  • TOM MCNEILLY,
  • Robin Pakeman,
  • Amy Sweeney,
  • Dan Nussey,
  • Amy Pedersen,
  • Andy Fenton
Andrew Dean
University of Liverpool

Corresponding Author:andrew.dean@liverpool.ac.uk

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Dylan Childs
The University of Sheffield
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Yolanda Corripio-Miyar
Moredun Research Institute
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Mike Evans
Moredun Research Institute
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Adam Hayward
Moredun Research Institute
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Fiona Kenyon
Moredun Research Institute
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Luke McNally
The University of Edinburgh
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TOM MCNEILLY
Moredun Research Institute
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Robin Pakeman
The James Hutton Institute
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Amy Sweeney
The University of Sheffield
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Dan Nussey
University of Edinburgh
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Amy Pedersen
The University of Edinburgh
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Andy Fenton
University of Liverpool
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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.
Submitted to Ecology and Evolution
23 Feb 2024Review(s) Completed, Editorial Evaluation Pending
30 Mar 2024Submission Checks Completed
30 Mar 2024Assigned to Editor
30 Mar 2024Review(s) Completed, Editorial Evaluation Pending
03 Apr 2024Editorial Decision: Accept