Why infectious disease research needs community ecology

Bringing ecology to infection The tools we use to investigate infectious diseases tend to focus on specific one-host–one-pathogen relationships, but pathogens often have complex life cycles involving many hosts. Johnson et al. review how such complexity is analyzed by community ecologists. Ecologists have the investigative tools to probe cause and effect relationships that change with spatial scale in multispecies communities. These techniques are used to monitor the ways in which communities change through time and to probe the heterogeneity that characterizes individuals, species, and assemblages—all issues that are also essential for disease specialists to understand. Science, this issue 10.1126/science.1259504 BACKGROUND Despite ongoing advances in biomedicine, infectious diseases remain a major threat to human health, economic sustainability, and wildlife conservation. This is in part a result of the challenges of controlling widespread or persistent infections that involve multiple hosts, vectors, and parasite species. Moreover, many contemporary disease threats involve interactions that manifest across nested scales of biological organization, from disease progression at the within-host level to emergence and spread at the regional level. For many such infections, complete eradication is unlikely to be successful, but a broader understanding of the community in which host-parasite interactions are embedded will facilitate more effective management. Recent advances in community ecology, including findings from traits-based approaches and metacommunity theory, offer the tools and concepts to address the complexities arising from multispecies, multiscale disease threats. ADVANCES Community ecology aims to identify the factors that govern the structure, assembly, and dynamics of ecological communities. We describe how analytical and conceptual approaches from this discipline can be used to address fundamental challenges in disease research, such as (i) managing the ecological complexity of multihost-multiparasite assemblages; (ii) identifying the drivers of heterogeneities among individuals, species, and regions; and (iii) quantifying how processes link across multiple scales of biological organization to drive disease dynamics. We show how a community ecology framework can help to determine whether infection is best controlled through “defensive” approaches that reduce host suitability or through “offensive” approaches that dampen parasite spread. Examples of defensive approaches are the strategic use of wildlife diversity to reduce host and vector transmission, and taking advantage of antagonism between symbionts to suppress within-host growth and pathology. Offensive approaches include the targeted control of superspreading hosts and the reduction of human-wildlife contact rates to mitigate spillover. By identifying the importance of parasite dispersal and establishment, a community ecology framework can offer additional insights about the scale at which disease should be controlled. OUTLOOK Ongoing technological advances are rapidly overcoming previous barriers in data quality and quantity for complex, multispecies systems. The emerging synthesis of “disease community ecology” offers the tools and concepts necessary to interpret these data and use that understanding to inform the development of more effective disease control strategies in humans and wildlife. Looking forward, we emphasize the increasing importance of tight integration among surveillance, community ecology analyses, and public health implementation. Building from the rich legacy of whole-system manipulations in community ecology, we further highlight the value of large-scale experiments for understanding host-pathogen interactions and designing effective control measures. Through this blending of data, theory, and analytical approaches, we can understand how interactions between parasites within hosts, hosts within populations, and host species within ecological communities combine to drive disease dynamics, thereby providing new ways to manage emerging infections. The community ecology of disease. (A) Interactions between parasites can complicate management. Among Tsimane villagers, treatment of hookworms increases infections by Giardia lamblia. (B) Similarly, understanding how ecological communities of hosts assemble can help forecast changes in disease. Biodiversity losses can promote interactions between white-footed mice and deer ticks, leading to an increase in the risk of Lyme disease from Borrelia burgdorferi. [Credits: (A) A. Pisor, CDC, F. Dubs; (B) J. Brunner, T. Shears, NIH] 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.