Host Competence: An Organismal Trait to Integrate Immunology and Epidemiology

Abstract

The new fields of ecological immunology and disease ecology have begun to merge, and the classic fields of immunology and epidemiology are beginning to blend with them. This merger is occurring because the integrative study of host-parasite interactions is providing insights into disease in ways that traditional methods have not. With the advent of new tools, mathematical and technological, we could be on the verge of developing a unified theory of infectious disease, one that supersedes the barriers of jargon and tradition. Here we argue that a cornerstone of any such synthesis will be host competence, the propensity of an individual host to generate new infections in other susceptible hosts. In the last few years, the emergence of systems immunology has led to novel insight into how hosts control or eliminate pathogens. Most such efforts have stopped short of considering transmission and the requisite behaviors of infected individuals that mediate it, and few have explicitly incorporated ecological and evolutionary principles. Ultimately though, we expect that the use of a systems immunology perspective will help link suborganismal processes (i.e., health of hosts and selection on genes) to superorganismal outcomes (i.e., community-level disease dynamics and host-parasite coevolution). Recently, physiological regulatory networks (PRNs) were cast as whole-organism regulatory systems that mediate homeostasis and hence link suborganismal processes with the fitness of individuals. Here, we use the PRN construct to develop a roadmap for studying host competence, taking guidance from systems immunology and evolutionary ecology research. We argue that PRN variation underlies heterogeneity in individual host competence and hence host-parasite dynamics.

Host stress hormones alter vector feeding preferences, success, and productivity

“…In general, understanding the ramifications of individual host stress biology for community disease risk is important, as host organisms are forced to endure or exploit increasingly modified areas [60]. As interindividual variation in competence is likely to vary extensively among hosts, disease risk may be greater than predicted based on current models [61] because of the disproportionate effects of some individuals on vector feeding and subsequent productivity when hosts are stressed [62,63]. …”

Extreme Competence: Keystone Hosts of Infections

“…We hope this framework helps reveal new forms of EC and informs and improves management of disease risk. promising research paths (Boxes 1 and 2 ) to reveal how hosts become so competent; a complement to other recent efforts [7,8]. We anticipate that this framework will be of value because it links disease processes within and among individual hosts for most host-parasite systems [4].…”

“…In Figure 1, we provide a framework for decomposing host competence into four componentsexposure, susceptibility, suitability and transmissibilitythat should be amenable to studying EC, including revealing novel forms of EC if they exist. Although these aspects of competence are coarse and multifaceted, just as with terms that comprise n, they are amenable to description at the individual level and even decomposable to their physiological bases [7,8]. So as to ground our framework in familiar territory, we collected data and plotted frequency distributions of all four aspects of host competence for two different infections: malaria parasites and lung nematodes ( Figure 1).…”

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

“…the ability to inhibit or reduce infection) or competence (i.e. the ability to transmit new infections to susceptible hosts or vectors) could be particularly informative, as these traits provide mechanistic links between within‐ and between‐host infection processes (Martin, Burgan, Adelman, & Gervasi, ; Roy & Kirchner, ) and may be less prone to the sampling biases found in global parasite datasets (Han, Kramer, & Drake, ).…”