The characteristics that make C. elegans an attractive experimental model reflect its survival strategy in the soil. Survival strategies have classically been considered in terms of “r-selection versus K-selection,” in which reproductive scheduling is selected on the basis of mortality rates and environmental stability. In unstable environments with high mortality rates, r-selection favors rapid development and early reproduction, whereas in stable environments with low mortality rates, K-selection favors genotypes resulting in slower development, larger size, longer reproductive period, and longer life span. The soil is presumably an unstable environment, with an uneven distribution of microbial food and considerable risk of death from environmental fluctuations in temperature or moisture, or from encounters with predators such as nematode-trapping fungi (Gray 1988).

C. elegans is itself a voracious predator that will eat anything that fits in its mouth. In the laboratory, it converts E. coli into C. elegans with an efficiency of nearly 50% (Lewis and Fleming 1995). In the soil, it apparently seeks to consume all available resources as quickly as possible as a means to overgrow its competitors. Both the rapid life cycle (14-hour embryogenesis and 36-hour postembryonic development through four larval stages, L1—L4 to the adult at 25°C) and large brood size favor this strategy, but a compromise must be reached between these two traits. The hermaphrodite is protandrous, first producing sperm in the late L4 stage then turning to the production of oocytes as an adult (L'Hernault; Schedl; both this volume). The adult is structurally a female, with its previously produced sperm stored in its spermathecae. The typical hermaphrodite produces many more oocytes than sperm, so the size of the brood is limited by the number of sperm. Oocyte production is stimulated by mating with males; a single hermaphrodite has the potential to produce more than 1000 progeny when mated. Why does the hermaphrodite not maximize its reproduction by producing more sperm? With the protandrous reproductive system, producing more sperm delays the onset of egg laying, effectively slowing the generation time. In this case, more is not better (Hodgkin and Barnes 1991).

Given its “boom and bust” strategy of rapid habitat depletion (consumption of all microbial food resources), an effective mechanism for dispersal to more favorable soil locations is important for evolutionary success. This is a predicament shared with nematode parasites that must migrate from one host to another through a harsh environment that will not support growth (Evans and Perry 1976). The nondeveloping dauer ("enduring") stage of C. elegans and analogous third-stage “infective” larvae of parasitic species are specialized to perform the needed dispersal function (Blaxter and Bird, this volume). In many parasites, the dauer larva is an obligate stage of diapause, whereas in C. elegans, it is facultative. Dauer larvae are not formed as long as the food supply is sufficient to support continued growth of the population, but as the food supply is diminished, dauer larvae are formed at the second larval molt (Riddle, this volume). Preparation for the nonfeeding dauer stage involves alteration of energy metabolism and accumulation of fat in intestinal and hypodermal cells; dauer-specific behaviors are specialized to favor dispersal. Dauer larvae can survive for many months, approximately ten times the normal life span, and when they encounter food, they resume development. Thus, C. elegans may successfully migrate through sparse soil resources from one region of microbial bloom to another.

Successful dauer dispersal is favored by hermaphrodite reproduction, since a single animal can establish a new population. Hence, the boom and bust lifestyle may be an important factor contributing to the persistence of hermaphrodite reproduction despite the normally deleterious effects of inbreeding. C. elegans males are rarely, if ever, isolated from soil, so if dauer dispersal is a prominent phase in the natural habitat, most populations may be clonal. This survival strategy selects against the accumulation of genetic load. In fact, neither inbreeding depression nor hybrid vigor (heterosis) has been observed in C. elegans (Johnson and Wood 1982; Johnson and Hutchinson 1993). The lack of heterosis eliminates a major complication for analysis of interstrain crosses and is particularly important for genetic analysis of life history traits such as life span, which is acutely dependent on the overall health of the organism. The short (2-week) life span of C. elegans and the availability of mutants with greatly increased longevity have stimulated its use as a model for research on aging (Kenyon, this volume).

If the simple scenario of dauer dispersal followed by clonal reproduction is correct, one might predict that C. elegans should reproduce by parthenogenesis rather than sex. The origin and evolution of sex, in fact, remain a controversial issue in evolutionary biology, but sex is generally rationalized as a necessary means to obtain favorable recombinant genotypes. In C. elegans, XO males arise spontaneously in XX hermaphrodite populations by means of X chromosome nondisjunction at a frequency of about 0.1% (Hodgkin et al. 1979; Meyer, this volume). The males mate with hermaphrodites (Emmons and Sternberg, this volume) to produce a 1:1 ratio of male and hermaphrodite cross-progeny, but additional hermaphrodites are almost always produced by selfing. Hence, the sex ratio is skewed toward the hermaphrodite. Petri dish populations starve before males have had time to cross sufficiently with a hermaphrodite to maximize the male to hermaphrodite ratio. In these small laboratory populations, males normally disappear after a few generations if the sex ratio is not actively maintained.

Choice of reproductive mode may be a simple matter of economics. Limited resources in nature may favor hermaphrodite reproduction, but more uniform environments, such as a compost heap that supports a large population originating from numerous individuals (reproducing for many generations prior to dauer dispersal), may be more favorable for crossing. It pays to be a hermaphrodite if there are diminishing returns in producing gametes. In other words, producing twice as many gametes may not produce twice as many surviving progeny if those progeny simply compete with one another for limited food or space. In contrast, an abundance of food would favor crossing with males to maximize the number of offspring. The choice between hermaphroditic and gonochoric (dioecious) reproduction may allow C. elegans to proliferate in a spectrum of soil environments.