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From Tolerance to Transmission: Linking Within-Individual to Community-Level Disease Processes

Hosts have two main strategies for coping with infections: resistance and tolerance. Resistance is aimed at preventing or eliminating parasites, whereas the goal of tolerance is to maintain performance regardless of parasite burden. The balance between resistance and tolerance within a host may mediate host competence, or the propensity of a host to infect other hosts or vectors. Hosts with high tolerance and low resistance to an infection, for instance, may be highly competent and possess the greatest potential to act as superspreaders. These superspreading hosts will contribute disproportionately to transmission, thus posing the greatest risk to other hosts within a population or community. Understanding the drivers of heterogeneity in host competence therefore has broad implications for the management of infectious diseases in nature.
Host tolerance is typically quantified as the slope of the relationship between host performance and parasite burden. The majority of host tolerance studies have been conducted at the level of genotypes, populations and species. Individual hosts often exhibit variation in competence, with some individuals contributing more or less to transmission than the population/species average. Despite the clear importance of understanding tolerance at the individual-level, such studies are rare and may be particularly challenging in field contexts due to the need for repeated performance-burden measurements. I used the house sparrow (HOSP) – West Nile virus (WNV) system to investigate differences among two alternative approaches to estimating individual tolerance: the scope and position methods. The scope method estimates tolerance traditionally as the slope of multiple performance-burden measurements over time within an individual; alternatively, the position method required only one measurement for each individual, thus characterizing tolerance via among-individual variation in host defense. We found strong relationships between scope and position estimates of individual tolerance, suggesting that the position method may be an appropriate proxy to use in field studies. I also compared tolerance estimates derived from different metrics of performance. There were weak correlations among these estimates of tolerance, implying that tolerance estimated by measuring a single trait may not be indicative of tolerance at the level of the whole individual or their contribution to disease processes.
Understanding the physiological mediators of host competence may help to pinpoint at-risk and risky individuals (or genotypes, populations and species) within natural communities, thus facilitating the development of more targeted disease management strategies. Cytokines and glucocorticoids have been identified as potent mediators of host defense. Pro-inflammatory cytokines may act to promote resistance, whereas anti-inflammatory cytokines and glucocorticoids tend to mediate host tolerance. I investigated the dynamics of pro-inflammatory cytokine IFN-γ, anti-inflammatory cytokine IL-10, and the major avian…