Host resources and parasite traits interact to determine the optimal combination of host parasite-mitigation strategies.

Autor: Dean AD; Institute of Infection, Veterinary and Ecological Sciences University of Liverpool Liverpool UK., Childs DZ; School of Biosciences The University of Sheffield Sheffield UK., Corripio-Miyar Y; Department for Disease Control Moredun Research Institute Penicuik UK., Evans M; Department for Disease Control Moredun Research Institute Penicuik UK.; The University of Edinburgh Royal (Dick) School of Veterinary Studies Roslin UK.; Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK., Hayward A; Department for Disease Control Moredun Research Institute Penicuik UK., Kenyon F; Department for Disease Control Moredun Research Institute Penicuik UK., McNally L; Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK., McNeilly TN; Department for Disease Control Moredun Research Institute Penicuik UK., Pakeman RJ; The James Hutton Institute Aberdeen UK., Sweeny AR; School of Biosciences The University of Sheffield Sheffield UK.; Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK., Nussey DH; Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK., Pedersen AB; Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK., Fenton A; Institute of Infection, Veterinary and Ecological Sciences University of Liverpool Liverpool UK.
Jazyk: angličtina
Zdroj: Ecology and evolution [Ecol Evol] 2024 Jun 19; Vol. 14 (6), pp. e11310. Date of Electronic Publication: 2024 Jun 19 (Print Publication: 2024).
DOI: 10.1002/ece3.11310
Abstrakt: 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. The effectiveness of a strategy depends on interactions between, for example, resource availability, parasite traits (virulence, life-history) and the host itself (nutritional status, immunopathology). 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. 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. Choice of parasite mitigation strategy has profound consequences for hosts, impacting their condition, survival and reproductive success. We show that 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.
Competing Interests: The authors declare no conflicts of interest.
(© 2024 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)
Databáze: MEDLINE