Why infectious disease research needs community ecology

Abstract

Infectious diseases often emerge from interactions among multiple species and across nested levels of biological organization. Threats as diverse as Ebola virus, human malaria, and bat white-nose syndrome illustrate the need for a mechanistic understanding of the ecological interactions underlying emerging infections. We describe how recent advances in community ecology can be adopted to address contemporary challenges in disease research. These analytical tools can identify the factors governing complex assemblages of multiple hosts, parasites, and vectors, and reveal how processes link across scales from individual hosts to regions. They can also determine the drivers of heterogeneities among individuals, species, and regions to aid targeting of control strategies. We provide examples where these principles have enhanced disease management and illustrate how they can be further extended.

Fig. 1. The community ecology of infectious disease

(A to C) Co-infection by nematodes (A) increases host mortality due to bovine TB (B) among African buffalo (C) (63). (D to F) Tsimane villagers in Bolivia (D) reveal negative correlations between Giardia lamblia (E) and Ascaris lumbricoides (F), where deworming increased Giardia (99). (G and H) For tick-borne encephalitis (G), 93% of transmission events involve large-bodied, male yellow-necked mice (H), which constitute <20% of the population (53). (I and J) For humans, disproportionate contact among individuals (I) led to “superspreading events” for SARS (J) (50). (K to N) Among-species heterogeneities can alter community-wide transmission. Crayfish plague (K) introduced to Europe with highly susceptible red swamp crayfish (L) led to native crayfish declines; biodiversity losses tend to promote interactions between ticks and white-footed mice (M), which are highly competent hosts for Borrelia burgdorferi (N) and influence production of infected ticks that transmit Lyme borreliosis (65). [Image credits: [(A), (E), (I), (J)] CDC, (B) R. Grencis, (C) Y. Krishnappa, (D) A. Pisor, (F) F Dubs, (G) (100) (H) V. Dostál, (K) T. Vrålstad, (L) F Pupin, (M) J. Brunner, (N) NIH]

Fig. 2. Ecological hierarchies applied to host-parasite interactions and analogous processes in community ecology

The range of scales includes within-host (“parasite infracommunity,” often dominated by parasite-parasite and parasite-immune system interactions); between-host (“parasite component community,” population biology); among species (“parasite supracommunity,” community ecology); and across regions (macroecology and disease biogeography). The different colored squares represent different parasite species; the text at the right and left highlights the relevant processes from community ecology and disease ecology, respectively. The potential importance for interactions and feedback across these scales represents an essential research frontier in the field of disease community ecology.

Fig. 3. Parasite community assembly depends on a combination of ecological selection, ecological drift, and dispersal

(A) After input via dispersal (indicated as arrows from the parasite regional pool), parasite establishment depends on ecological selection: different species (mice versus prairie dogs) select for different parasites according to genetics, behavior, immune status, and other host properties (including vaccination status or drug presence). Dashed arrows indicate failed infection. Deterministic, within-host parasite interactions (indicated by + and − signs) are an additional niche-based influence on parasite communities; positive parasite interactions (facilitation) are indicated by solid arrows; negative interactions are indicated by dashed arrows. (B) Parasite community assembly is also influenced by ecological drift (stochasticity), particularly when colonizing populations are small or the outcome of parasite interactions depends on their order of arrival (“priority effects”). As a result, parasite communities can appear random with respect to host species or type, even if strongly affected by species interactions. (C) High rates of dispersal can swamp niche effects and overwhelm stochasticity, resulting in more similar parasite communities across hosts, regardless of host species. For simplicity, no feedback loops are shown from the individual hosts back to the parasite pool, although understanding such feedbacks represents an important research priority (Fig. 2).

Fig. 4. How community ecology can inform infectious disease management

(A) Using community ecology–based management strategies for infectious disease. Levels of ecological organization are shown in the middle, and colored arrows indicate the ecological processes that connect these levels. Parasite dispersal connects scales going up through the hierarchy; parasite establishment connects scales moving down the hierarchy. Blue arrows indicate the relative importance of offensive strategies (preventing parasite dispersal) and defensive strategies (preventing parasite establishment), with darker shades reflecting greater importance. (B) Management strategies focused on reducing spillover from wildlife to humans (zoonosis) and from humans to wildlife (anthronosis or reverse zoonosis). Probability of spillover and subsequent spread of infection can be reduced through four major strategies: (i) Control may focus on reducing disease prevalence in reservoir hosts; for instance, vaccine baits have been successfully used to eliminate rabies from several European countries (80). (ii) Contact rates can be reduced between humans and wild animals (8); for example, limiting the proximity between humans and wildlife can reduce spillover of human illnesses such as measles, tuberculosis, and MRSA to wildlife. (iii) Zoonotic risk can be reduced by lowering the probability of infection when contact is unavoidable or unpredictable. For instance, some human dengue vaccine candidates provide cross-protection against sylvatic dengue viruses, which naturally circulate in nonhuman primates (85). (iv) When spillover does occur, regional control strategies—including isolation of infected populations, dispatching of medical personnel and aid, and enhanced border control—can be used to prevent disease transmission across borders.