A Model for Evolutionary Ecology of Disease: The Case for Caenorhabditis Nematodes and Their Natural Parasites

Abstract

Many of the outstanding questions in disease ecology and evolution call for combining observation of natural hostparasite 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.

Host genetic drift and adaptation in the evolution and maintenance of parasite resistance

“…Very few experiments have tested adaptation of C . elegans to their local parasites directly (Gibson & Morran, 2017). It may be that in nature, C .…”

Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

“…Because C. elegans will continue to serve as the workhorse for most studies of male biology, it is important to consider the generality of discoveries made with the genetic background of N2-a strain known to harbor numerous adaptations to laboratory conditions having pleiotropic effects (Zhao et al 2018)-and yet with little understanding of their implications for male traits. More generally, a challenge for C. elegans laboratory experimental power remains: how to link exciting laboratory discoveries to the more complex natural environment, which includes both biotic and abiotic heterogeneity (Gibson and Morran 2017;Zhang et al 2017). With abundant questions at the ready, both evolutionary and mechanistic, future studies of C. elegans males that leverage the system's extensive experimental resources are poised to discover novel biology, and to inform profound questions about animal function and evolution.…”

“…Non-nematode field studies provide the majority of empirical evidence supporting the Red Queen model (Hartfield and Keightley 2012;Lively and Morran 2014), but many field systems are ill-suited to direct manipulative tests of its predictions. Utilizing C. elegans as a host of parasites, including bacteria, viruses, microsporidia, and fungi (reviewed in Gibson and Morran 2017 ;Schulenburg and Felix 2017), provides researchers the opportunity to use experimental evolution to test directly diverse predictions and assumptions of the Red Queen model.…”

The impact of intragenomic rRNA variation on metabarcoding‐derived diversity estimates: A case study from marine nematodes

“…Recovery of some types of nontarget DNA can provide novel scientific insights, especially if this information is explicitly linked with specimen‐level data. For example, many nematodes and microbial metazoan species are known to harbor microbial symbionts and parasites, such as microsporidian taxa infecting nematodes in both soil and marine environments (Gibson & Morran, 2017; Sapir et al, 2014). One recent metabarcoding study also reported distinct community profiles of protist taxa associated with metazoan DNA extracts (dominated by parasitic and pathogenic species, Geisen, Laros, Vizcaíno, Bonkowski, & de Groot, 2015) compared to protist mock community assemblages, indicating that host‐associated microbial pathogens remain poorly characterized despite their seemingly common occurrence in natural habitats worldwide.…”