Abstract
Many of the outstanding questions in disease ecology and evolution call for combining observation of natural host-parasite populations with experimental dissection of interactions in the field and the laboratory. The "rewilding" of model systems holds great promise for this endeavor. Here, we highlight the potential for development of the nematode Caenorhabditis elegans and its close relatives as a model for the study of disease ecology and evolution. This powerful laboratory model was disassociated from its natural habitat in the 1960s. Today, studies are uncovering that lost natural history, with several natural parasites described since 2008. Studies of these natural Caenorhabditis-parasite interactions can reap the benefits of the vast array of experimental and genetic tools developed for this laboratory model. In this review, we introduce the natural parasites of C. elegans characterized thus far and discuss resources available to study them, including experimental (co)evolution, cryopreservation, behavioral assays, and genomic tools. Throughout, we present avenues of research that are interesting and feasible to address with caenorhabditid nematodes and their natural parasites, ranging from the maintenance of outcrossing to the community dynamics of host-associated microbes. In combining natural relevance with the experimental power of a laboratory supermodel, these fledgling host-parasite systems can take on fundamental questions in evolutionary ecology of disease.
Highlights
Many of the outstanding questions in disease ecology and evolution call for combining observation of natural host– parasite populations with experimental dissection of interactions in the field and the laboratory
In Lively et al (2014), several prominent researchers presented a sample of these outstanding questions: (i) Does host genetic diversity limit the spread of an infectious disease? (ii) Can selection by parasites maintain genetic diversity in host populations? (iii) What are the effects of environmental variation and community context on the interaction between a host and parasite? (iv) Is the one host–one parasite framework instructive for understanding the real-world interaction of multiple hosts and multiple parasites? (v) What is the effect of a host’s microbiota on the evolution and ecology of a host– parasite system? These questions highlight the importance of studying disease at both the individual and population levels
The authors proposed that one approach to answering the outstanding questions of disease evolution and ecology is the development of ‘‘new study systems. . .where natural populations can be used in laboratory experiments and/or where experimental studies can be conducted in the wild’’
Summary
In spite of a lack of natural parasites, model organisms serve as powerful systems in which to study the immunological and molecular basis of infection. This work was exciting because of the ease of genetic manipulation of both the host and the parasite This group of studies suggested that the interactions of C. elegans with parasites that infect distant hosts (e.g. humans, crops) might provide insight into general mechanisms of infection and conserved components of host immunity. A wide range of behavioral and life history assays exist to test individual genotypes and phenotypes With these tools in hand, researchers can measure the fitness of specific alleles or genotypes by tracking changes in their frequencies within and between populations in real time. For C. elegans, life in the wild hinges on finding bacterial food sources, so variation in bacterial discrimination likely has natural relevance Such behavioral assays can be used in combination with feeding, mobility, and chemosensory mutants to dissect the contribution of parasite exposure to disease resistance. These studies suggest possible scenarios for the evolution of natural C. elegans populations in response to natural parasites
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