What Does Tolerance Mean for Animal Disease Dynamics When Pathology Enhances Transmission?

• Published in: Integrative and comparative biology 2019-11, Vol.59 (5), p.1220-1230
• Main Authors: Henschen, Amberleigh E., Adelman, James S.
• Format: Article
• Language: English
• Subjects: Animals; Anopheles - parasitology; Finches; Host-Parasite Interactions; Host-Pathogen Interactions; Influenza in Birds - pathology; Influenza in Birds - transmission; Influenza in Birds - virology; Malaria - parasitology; Malaria - pathology; Malaria - transmission; Malaria - veterinary; Mycoplasma gallisepticum - physiology; Mycoplasma Infections - microbiology; Mycoplasma Infections - pathology; Mycoplasma Infections - transmission; Mycoplasma Infections - veterinary; Orthomyxoviridae - physiology; Plasmodium - physiology; S2 The scale of sickness: how immune variation across space and species affects infectious disease dynamics
• ISSN: 1540-7063; 1557-7023
• DOI: 10.1093/icb/icz065

Host competence, or how well an individual transmits pathogens, varies substantially within and among animal populations. As this variation can alter the course of epidemics and epizootics, revealing its underlying causes will help predict and control the spread of disease. One host trait that could drive heterogeneity in competence is host tolerance, which minimizes fitness losses during infection without decreasing pathogen load. In many cases, tolerance should increase competence by extending infectious periods and enabling behaviors that facilitate contact among hosts. However, we argue that the links between tolerance and competence are more varied. Specifically, the different physiological and behavioral mechanisms by which hosts achieve tolerance should have a range of effects on competence, enhancing the ability to transmit pathogens in some circumstances and impeding it in others. Because tissue-based pathology (damage) that reduces host fitness is often critical for pathogen transmission, we focus on two mechanisms that can underlie tolerance at the tissue level: damage-avoidance and damage-repair. As damage-avoidance reduces transmission-enhancing pathology, this mechanism is likely to decrease host competence and pathogen transmission. In contrast, damage-repair does not prevent transmission-relevant pathology from occurring. Rather, damage-repair provides new, healthy tissues that pathogens can exploit, likely extending the infectious period and increasing host competence. We explore these concepts through graphical models and present three disease systems in which damage-avoidance and damage-repair alter host competence in the predicted directions. Finally, we suggest that by incorporating these links, future theoretical studies could provide new insights into infectious disease dynamics and host–pathogen coevolution.