Academic journal article Genetics

Experimental Evolution with Caenorhabditis Nematodes

Academic journal article Genetics

Experimental Evolution with Caenorhabditis Nematodes

Article excerpt

"With them, many important questions will be accessible to patient observers who do not fear long-term experiments." - Emile Maupas (1900)

OVER a century ago, Emile Maupas introduced the nematode Caenorhabditis elegáns to the scientific community with his report on a failed experiment aimed at testing the hypothesis that continual self-fertilization (selfing) should lead to population extinction (Maupas 1900). This goal was ultimately thwarted, as after nearly 50 generations of selfing, Maupas' C. elegáns culture collapsed due to an errant spike in temperature that led to abnormalities in development and reproduction independently of inbreeding effects. Maupas' experimental evolution study was inspired by an ongoing debate about the long-term sustainability of selfing as a reproductive strategy (Darwin 1876), and provides a particularly telling introduction to experimental evolution: the expected outcome (extinction) was achieved, but for the "wrong" reason, as it was not a result of selfing.

Experimental Evolution (EE) has long been used as the gold standard for testing evolutionary hypotheses about natural selection and genetic drift, estimating theoretical parameters regarding standing genetic variation, such as mutation and recombination rates, and, more recently, as a means for gene discovery. The main organismal models to which EE has been applied are mice, fruit flies, yeast, and bacteria (Rose and Lauder 1996; Bell 1997; Garland and Rose 2009; Kassen 2014). Despite the promising start by Emile Maupas (Maupas 1900), however, it was nearly 90 years before Caenorhabditis reappeared in EE research, during which time much evolutionary theory had been mathematically formalized.

Because of its relative newcomer status in EE research, we have barely begun to tap the potential of Caenorhabditis for elucidating the patterns and processes of evolution (Gray and Cutter 2014). But, as the community of Caenorhabditis evolutionary biologists has grown-now sufficiently large to merit regular meetings and dedicated stock and databases (Supplemental Material, Table S1 in File S1; Carvalho et al. 2006; Haag et al 2007; Braendle and Teotónio 2015)-so too has the array of evolutionary problems being investigated with experiments (Table 1 lists some of the studies that will be covered here).

Caenorhabditis are free-living bactivorous roundworms with over 25 species currently being cultured in the laboratory (Kiontke et al. 2011; Felix et al. 2014), although only C. elegans, C. briggsae, and C. remanei have been utilized in EE research. A distinctive feature of this group of nematodes is that facultative selfing evolved independently from ancestral obligatory outcrossing three times (Kiontke and Fitch 2005). C. elegans, C. briggsae, and C. tropicalis have a rare androdioecious reproduction system, with hermaphrodites capable of selfing, and of outcrossing with males, but not with other hermaphrodites. Hermaphrodites from these species are developmentally similar to females of related dioecious species, except for a period during germline specification and differentiation when sperm is produced and stored in the spermatheca prior to an irreversible switch to oogenesis at adulthood. These hermaphrodites are therefore self-sperm limited and can only fertilize all of their oocytes when mated by males (Barker 1992; Cutter 2004). Behaviorally, hermaphrodites have lost the ancestral ability to attract males, and are generally reluctant to mate until they have depleted their own self-sperm store (Lipton et al. 2004; Chasnov et al. 2007).

Our aim with this review is to present Caenorhabditis species as excellent models for EE. We first focus on the basic principles of EE, which apply more or less to any organism, and then introduce Caenorhabditis and related resources for their use in EE. We next explore the common goals and outcomes of EE studies in sections devoted to laboratory domestication and specific EE designs that address the fundamental processes of natural selection, genetic drift, mutation, segregation, and recombination. …

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