Extreme Competence: Keystone Hosts of Infections

Abstract

Individual hosts differ extensively in their competence for parasites, but traditional research has discounted this variation, partly because modeling such heterogeneity is difficult. This discounting has diminished as tools have improved and recognition has grown that some hosts, the extremely competent, can have exceptional impacts on disease dynamics. Most prominent among these hosts are the superspreaders, but other forms of extreme competence (EC) exist and others await discovery; each with potentially strong but distinct implications for disease emergence and spread. Here, we propose a framework for the study and discovery of EC, suitable for different host-parasite systems, which we hope enhances our understanding of how parasites circulate and evolve in host communities.

Keywords: disease; epidemic; infection; zoonosis.

Figure 1

Possible Forms and Mechanisms of Extreme Host Competence For a Figure360 author presentation of Figure 1, see the figure legend at https://doi.org/10.1016/j.tree.2018.12.009 The four frequency distributions for two host–parasite interactions (A and C) depict variation among individual hosts in a population for: (i) exposure to parasites; (ii) susceptibility to parasites; (iii) suitability of a host for a parasite; and (iv) transmissibility of parasites once infected. The composite of these traits is host competence. Panel A depicts existing information on competence for human and avian malaria (Plasmodium and Haemoproteus). Exposure and transmissibility both depend on vector biting rates and are strongly right skewed in humans. By contrast, susceptibility is universally high. Data from a wild tropical avian community suggest that most infections are chronic with most individuals maintaining parasite burdens insufficient for transmission to vectors (i.e., low suitability). In panel A, a malaria (vector) superattractor has high exposure risk, but it is unknown whether such hosts tend to have high or low suitability and transmissibility and thus act as superspreaders or superdiluters. Red and blue circles denote traits of two different individuals in all four stages of the host–vector–parasite interaction. Panel B depicts that superattracting could have either superdiluting or superspreading consequences depending on relationships between traits within hosts. White-filled symbols depict uninfected hosts, black-filled symbols depict infected hosts, blue and red symbols reflect alternate forms of competence, and green-shaded circles reflect host impacts on local transmission. In panel C, frequency distributions reflect data from invasive populations of cane toads (Rhinella marina) and their lung nematodes (Rhabdias pseudosphaerocephala). Exposure rates are high, except at the leading edge of the geographic range of this host. Susceptibility is also high (100% success rates in experimental infections), yet suitability is variable with some hosts capable of clearing worms and others less so. Transmissibility is high for most hosts. Whether a host with a high burden has high transmissibility depends on parasite-mediated effects on factors determining the behavior during and duration of the period over which hosts shed parasites. Red and blue triangles denote traits of the two different individuals in all four stages of the host–parasite interaction. Panel D depicts the two possible outcomes of different trait combinations. White-filled symbols depict uninfected hosts, black-filled symbols depict infected hosts, blue and red symbols reflect alternate forms of competence, and green-shaded circles reflect local risk. Also see the supplemental information online regarding the supporting material for this figure.

Figure I

A Few Examples of How Host Tolerance Could Contribute to Host Competence.