Academic journal article Genetics

From "The Worm" to "The Worms" and Back Again: The Evolutionary Developmental Biology of Nematodes

Academic journal article Genetics

From "The Worm" to "The Worms" and Back Again: The Evolutionary Developmental Biology of Nematodes

Article excerpt

THE small, laboratory-friendly nematodes of the genus Caenorhabditis were first developed as a system for genetic analysis of animal development by a few early champions. One of the first experimental studies on C. elegans was performed by Japanese American Hikokuro Honda, who found that sperm determine the sex of progeny, and discovered that oocyte meiosis is not completed until after fertilization (Honda 1925). Two decades later, the French biologist Victor Nigon and his American colleague Ellsworth Dougherty greatly extended this work (Nigon 1943; Dougherty and Nigon 1949; Ferris and Hieb 2015; Nigon and Félix 2017), aided by improvements in culture methodology by Briggs (1946). These workers set the stage for Sydney Brenner's breakthroughs with C. elegans (Brenner 1974, 2009). Along with French biologist Emile Maupas, who first described C. elegans (Maupas 1900), all of these early researchers were struck by the fact that, within a stereotypical body form, evolutionary variation in habitat choice, feeding strategy, reproductive mode, behavior, and anatomical details are rampant. Thus, research focusing on C. elegans was always complemented by the work of other nematologists working in other groups, such as other nematodes in the order Rhabditida (Figure 1) (Sudhaus 1976). It can therefore be fairly said that questions of biodiversity, the evolution of developmental processes, and their connections to ecology were very much lingering over the field even in the earliest days. The authors of this review represent examples of contemporary biologists who share their predecessors' fascination with the evolution of nematode development. Trained in the C. elegans paradigm, we and others take particular delight in gazing outward across the phylogeny, always on the lookout for new phenomena and explanations for how they evolved.

Unique Attributes of the Caenorhabditis System

Caenorhabditis offers an attractive set of attributes for evolutionary developmental biology (EDB, or "evo-devo"). First, it presents a highly simplified and stereotyped developmental system. Worms are transparent and have a small number of somatic cells formed by a predictable lineage (Sulston and Horvitz 1977; Kimble and Hirsh 1979; Sulston et al. 1983). This allows one to homologize and compare developmental processes at the resolution of individual cells (Zhao et al. 2008). Nevertheless, the major tissues of larger, more complex animals (e.g., muscles, integument, nerves, sensory cells, renal, digestive and reproductive organs, and immune cells) are present (see www.wormatlas.org). While zoologists of the past believed the simple anatomy of nematodes represented a primitive state, molecular phylogenetics (Figure 1) have generally supported the membership of the phylum Nematoda in the Ecdysozoan superphylum of protostomes (Giribet and Edgecombe 2017). This implies that nematodes' often miniature bodies are actually highly derived and highly specialized. An alternative interpretation to the C. elegans body, therefore, is that it is a sophisticated, "microchip animal" that evolved from a larger progenitor. Along the way, some ancestral regulators of animal development have been shed or modified. For example, Caenorhabditis have fewer Hox genes than other nematodes or more distantly related animals (Aboobaker and Blaxter 2003), and the hedgehog signaling pathway has both diverged in its roles (Bürglin and Kuwabara 2006; Soloviev et al. 2011) and been co-opted to form the core of the global sex determination pathway (Zarkower 2006). Simultaneously, proteins implicated in chemosensation, such as rhodopsin-related G protein-coupled receptors, have been amplified and diversified (Bargmann 2006).

A striking variable distinguishing some nematodes, such as Caenorhabditis, Pristionchus, and some other clade V taxa relates to sexual mode. Although the ancestral gonochoristic (male-female), obligately outcrossing mode is retained by most species, several have evolved a self-fertile hermaphrodite (Kiontke et al. …

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