Interspecific Contact and Competition May Affect the Strength and Direction of Disease-Diversity Relationships for Directly Transmitted Microparasites

Abstract

The frequency of opportunities for transmission is key to the severity of directly transmitted disease outbreaks in multihost communities. Transmission opportunities for generalist microparasites often arise from competitive and trophic interactions. Additionally, contact heterogeneities within and between species either hinder or promote transmission. General theory incorporating competition and contact heterogeneities for disease-diversity relationships is underdeveloped. Here, we present a formal framework to explore disease-diversity relationships for directly transmitted parasites that infect multiple host species, including influenza viruses, rabies virus, distemper viruses, and hantaviruses. We explicitly include host regulation via intra- and interspecific competition, where the latter can be dependent on or independent of interspecific contact rates (covering resource utilization overlap, habitat selection preferences, and temporal niche partitioning). We examine how these factors interact with frequency- and density-dependent transmission along with traits of the hosts in the assemblage, culminating in the derivation of a relationship describing the propensity for parasite fitness to decrease in species assemblages relative to that in single-host species. This relationship reveals that increases in biodiversity do not necessarily suppress frequency-dependent parasite transmission and that regulation of hosts via interspecific competition does not always lead to a reduction in parasite fitness. Our approach explicitly shows that species identity and ecological interactions between hosts together determine microparasite transmission outcomes in multispecies communities.

Host traits and competitive ability jointly structure disease dynamics and community assembly

“…Our analyses are broadly consistent with previous work (Begon et al, ; Bowers & Turner, ; Greenman & Hudson, , ; O'Regan et al, ; Strauss et al, ), showing that competition, parasitism and their relationships affect not only disease dynamics, but also the dynamics of host communities. We extend this thinking to include the effects of disease on community composition by exploring a wider range of ecological scenarios and by linking disease and community dynamics to specific traits (Figures and ).…”

“…Parasitism has, analogously to competition, been invoked as a force driving selection, population dynamics, community composition and food web dynamics (Dobson, Lafferty, & Kuris, ). Extensive theoretical work has shown that infectious disease can affect host communities and host coexistence outcomes (Greenman & Hudson, , ; Holt & Pickering, ; Joseph, Mihaljevic, Orlofske, & Paull, ; Mordecai, ; O'Regan, Vinson, & Park, ). For example, in a relatively simple system with two self‐regulating host species that share a parasite, various coexistence outcomes are possible, including the elimination of one host, or the coexistence of both hosts in the presence or absence of the parasite (Begon, Bowers, Kadianakis, & Hodgkinson, ).…”

“…Additionally, when interspecific competition is incorporated into a similar model, the coexistence outcomes for both hosts and parasites are dependent on the strength of interspecific competition and the strength of interspecific disease transmission (Bowers & Turner, ). Moreover, O'Regan et al () have shown that these relationships between contact rates and competition can affect diversity and disease spread in a directly transmitted parasite system. While it is evident that infectious disease can affect host communities, the interplay between disease, host diversity and host interactions can be complex.…”

“…Parasitism and competition co-occur in many populations and communities, and in some cases, competitive ability may be correlated with host traits that are important to host-parasite dynamics (O'Regan et al, 2015;Strauss, Bowling, Duffy, Cáceres, & Hall, 2018;Strauss et al, 2015). Individuals that are most proficient at spreading disease may be strong (positive correlation), intermediate (no correlation) or weak competitors (negative correlation) depending on the mechanisms underlying this relationship.…”

“…Since complex interactions and feedbacks are likely when certain traits are correlated with competitive ability in a community, the ability to intuit the resulting effects of these correlations on community dynamics may break down. Fortunately, the diverse theoretical work that has investigated the effects of parasites in communities (Begon et al, 1992;Bhattacharya & Martcheva, 2016;Bowers & Turner, 1997;Fenton & Brockhurst, 2008;Fenton, Streicker, Petchey, & Pederson, 2015;Holt & Pickering, 1985;Joseph et al, 2013;Mihaljevic, Joseph, Orlofske, & Paull, 2014;O'Regan et al, 2015;Strauss et al, 2015) provides an excellent framework to approach these complex questions.…”