sign in sign up
<<
Home , Caenorhabditis elegans

Magazine R965

Does Hydra have an associated one of us (M.A.F.) has experienced, microbiome? Yes, it does. Like Primer long years of skimming through soil the human gut, Hydra is home to samples from all corners of the world an array of bacterial residents. The have been frustratingly fruitless. composition of the microbiome for a The natural history Human-made heaps are a particular of Hydra seems to be relatively reliable source of C. elegans, quite stable. How the microbiome is of allowing the first ‘semi-natural’ studies maintained and what it contributes to elegans on the extent and spatial structure the are important questions that of its genetic diversity, population are starting to be addressed. Hydra Marie-Anne Félix1 dynamics and outcrossing rate. Several is a much simpler model for studying and Christian Braendle2 more years had to elapse before host/microbe interaction than C. elegans was regularly sampled from vertebrate models such as humans In the laboratory, the more undisturbed habitats. Thanks to and mice. Caenorhabditis elegans lives on repeated scouring of various microbe- the surface of nutrient agar in Petri rich samples in diverse habitats, we I’ve heard that Hydra is immortal; dishes, feeding on a lawn of the and others have found C. elegans is that true? It appears so. Daniel auxotroph strain OP50, an and other Caenorhabditis species in Martinez followed 100 adult Hydra mutant strain. This different types of rotting plant material, for four years, discarding the buds sentence sums up the fundamentals such as fruits, stems and flowers as they were produced. The parental of C. elegans ecology, as most of us (Figure 1). did not undergo age-related know it. While over 15,000 articles on Current data thus indicate that . Individual cells die in diverse biological aspects of C. elegans C. elegans is not principally a soil Hydra, but the organism as a whole attest to the worm’s undisputable nematode, but rather a colonizer does not have a fixed life-span. virtues as a major , of various microbe-rich habitats, There is, however, evidence that its biology in the wild remains in particular decaying plant matter. some species of Hydra undergo mysterious. To properly interpret and Improbable as it may seem, rotting senescence following sexual fully understand the available wealth of fruit/plant material thus unites three . associated with genetic, molecular and other biological major lab model organisms in the same the aging process in other animals observations made in the laboratory, ecological context: Saccharomyces have not yet been examined in Hydra, it will be important to know its natural cerevisiae, melanogaster but clearly one would like to know history and to place the species in its and C. elegans. What the three species more in this regard. ecological and evolutionary context. share is a rapid lifecycle, a likely legacy With the aim of connecting the from their boom-and-bust lifestyle Where can I find out more? discoveries that have been made about exploiting ephemeral resources. Chapman, J.A., Kirkness, E.F., Simakov, O., C. elegans biology to its ‘real life’, we Hampson, S.E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P.G., Borman, J., shall discuss recent studies on the Phylogenetic context and Busam, D., et al. (2010). The dynamic worm’s natural habitat and population biogeography of Hydra. Nature 464, 592–596. biology, and outline key issues in The Caenorhabditis presently Fraune, S., and Bosch, T.C. (2007). Long-term maintenance of species-specific bacterial attaining a modern natural history comprises around 25 described microbiota in the basal metazoan Hydra. of C. elegans. species, of which only seven have Proc. Natl. Acad. Sci. USA 104, 13146–13151. Hydra genome browser: http://hydrazome. been maintained as live or frozen metazome.net/ Natural habitat lab stocks. Their natural habitat Martínez, D.E. (1998). Mortality patterns suggest Where does C. elegans live? Efforts and ecological specificities are very lack of senescence in hydra. Exp. Gerontol. 33, 217–225. to systematically sample C. elegans poorly understood, mainly because Martínez, D.E., Iñiguez, A.R., Percell, K.M., Willner, in nature were initially hampered by many species have been isolated J.B., Signorovitch, J., and Campbell, R.D. the absence of precise ecological only once or twice. The exception is (2010). Phylogeny and biogeography of Hydra (Cnidaria: Hydridae) using mitochondrial and information on the whereabouts of C. drosophilae, which seems to be nuclear DNA sequences. Mol. Phylogenet. this tiny roundworm, which reaches ecologically specialized: this species Evol. 57, 403–410. a length of only 1–2 mm as an adult. has been found on rotten Saguaro Trembley, A. (1744). Mémoires, pour Servir à l’Historie d’un Genre de Polypes d’Eau Douce, The first description ofC. elegans cactus in Arizona, in a phoretic à Bras en Forme de Cornes (Leiden: Jean and and its site of isolation by the French (transport) association with the fly Herman Verbeek). van Leeuwenhoek, A. (1996). The collected letters zoologist Emile Maupas did not Drosophila nigrospiracula, allowing of Antoni van Leeuwenhoek. In The Collected simplify this task: “J’ai rencontré à dispersal between cactus plants. Letters of Antoni van Leeuwenhoek, Volume deux reprises cette espèce dans les Although the Caenorhabditis species XIV, L.C. Palm, ed. (Lisse, Berwyn, PA: Swets and Zeitlinger), pp. 169–173. environs d’Alger: une première fois en forming the ‘Elegans-group’ are Wittlieb, J., Khalturin, K., Lohmann, J.U., mai, la seconde en novembre 1897. morphologically similar, they are highly Anton-Erxleben, F., and Bosch, T.C.G. (2006). Elle vit dans l’humus gras” divergent at the genetic level. To what Transgenic Hydra allow in vivo tracking of individual stem cells during . (“I came twice across this species in degree this divergence is linked to Proc. Natl. Acad. Sci. USA 103, 6208–6211. the surroundings of Algiers: a first time alternative ecological specialization of in May, a second time in November different species remains so far largely 1897. It lives in rich humus”, Maupas unexplored. Department of Biological Chemistry and the Center University wrote in 1900). From then on, The recent burst of world-wide of California, Irvine, CA 92697-1700, USA. C. elegans was referred to as a soil sampling from rotting plant material *E-mail: [email protected] nematode in the literature. Yet, as has yielded many new Caenorhabditis Current Biology Vol 20 No 22 R966

Proliferation Proliferation develop into adult on rotting fruit Dispersal on rotting fruit that enter reproductive diapause. In or stem via or stem addition, in the adult stage, individuals carrier may promptly stop laying embryos upon food depletion, while the embryos Nictation behaviour remaining in the continue to mature, hatch internally and feed on the decaying mother during the initial larval instars — perhaps a strategy guaranteeing that a small number of internally developing larvae reach the dauer stage. Finally, if starved, C. elegans may also diapause in the L1 stage — the only stage that Adult Adult Embryos Embryos survives freezing over years. Whether this freezing resistance is ecologically Direct Dauer Direct d L4 reproductive L1 L2d L4 reproductive L1 L2d d relevant, for example for survival during cycle(s) cycle(s) cold winters in temperate zones, L2 L2 L3 L3 is not known. Many developmental genetic studies Current Biology have investigated dauer formation — a prime example of apparently Figure 1. The life cycle of C. elegans in its natural habitat. adaptive phenotypic plasticity. In the C. elegans proliferates in various types of rotting plant material, such as fruits. Dauer larvae are the stress-resistant, alternative L3 stage, induced by crowding, food depletion and high lab, dauer entry is induced during the temperature. Dauer larvae may actively disperse to colonize new food sources. Alternatively, L1–L2 stages by synergistic effects of their nictation behaviour — standing on their tail on pointy surfaces such as moss leaves and low food concentration, pheromone waving — may allow them to attach to disperse via carriers, such as slugs, snails, isopods or sensation at high population myriapods, until a new food source is encountered, where development resumes. L1–L4, larval densities, and high temperature. This stages; d, ; L2d, pre-dauer larva in the L2 stage. developmental choice involves sensory regulation through the TGF-ß, species and given a clearer picture details, see http://blog.wormbase. and steroid pathways. Among natural of the distribution of C. elegans and org/?s=sister+prize). isolates of C. elegans, substantial relatives. There are, however, still genetic variation is found in the important geographical sampling Development, diapause and dispersal sensitivity to entering the dauer stage biases — often coinciding with past When well-fed in the laboratory, at in response to given amount of dauer holiday or congress locations of 20°C, C. elegans passes in about 3.5 pheromone or temperature. Exit from zealous C. elegans naturalists. to 4 days through a short embryonic the dauer stage is a key, irreversible C. elegans is cosmopolitan, being developmental period, followed by decision made at the individual level. found on most continents and four juvenile stages (named L1 to L4), Lab studies indicate that high food many isolated islands. It shares the separated by a phase of lethargus concentration and low temperature are temperate regions with two relatives of and moulting. C. elegans, or rather the cues favouring dauer exit, but natural the ‘Elegans group’, C. briggsae (also a reference lab strain N2, can develop cues may differ and are not necessarily facultative self-fertilizing species) and and reproduce at a wide range of symmetric with those for dauer entry. C. remanei (a male–female species). temperatures, but development halts In a given substrate sample, C. elegans Sampling in the tropics has yielded below 8°C and the animals become and other Caenorhabditis species, such C. briggsae, C. brenneri, and many sterile above 27°C. as C. briggsae, may often be found as yet undescribed Caenorhabditis Critical life-history choices likely primarily in the dauer stage, whereas species, but C. elegans relatively rarely. reflect adaptations to the fluctuating other rhabditid species are actively The recent discovery of these and ephemeral natural habitat of proliferating. Understanding the cues novel Caenorhabditis species C. elegans. At several specific points of that regulate dauer entry and exit in the has considerably enhanced the development, the animals may undergo wild, and how these responses evolve phylogenetic context of C. elegans a developmental arrest, known as in different environmental contexts, are and provided a tool for novel genomic diapause, characterized by reduced thus highly relevant, but unresolved and phenotypic studies, such as metabolism and increased stress issues of C. elegans ecology. genetic analysis of species hybrids. resistance. In young larvae, various C. elegans dauer larvae can be For example, C. briggsae has several types of stress induce the formation of isolated either from rotten plant close relatives, including its present dauer larvae as an alternative L3 stage, material after peaks of population sister, C. sp. 9, a male–female species evolutionarily related to the infective expansion, or from invertebrate with which it can form fertile hybrids. stage of parasitic (Figure 1; carriers, such as isopods (Figure 1). In Unfortunately, the search for a sister see below). Dauer larvae are resistant contrast to other nematode species, species of C. elegans has so far to many stressors and can survive C. elegans does not seem to have been without result — this despite without food for several months, whilst highly specific associations: carriers a tantalizing cash-and-naming prize adults usually live about two weeks. include various species of slugs, snails, offered to anyone who finds one (for When L4 larvae are starved, they may isopods, myriapods and perhaps Magazine R967 some and mites. Crucial recolonization (see below), may also between genetically distinct, isolated experiments to decode C. elegans have favoured the evolution of , clonal populations, thus causing ecology will include quantitative, which assures reproduction of an outbreeding depression. A particular unbiased sampling of a wide range isolated individual. case is the widespread incompatibility of to identify carrier The reproductive between two haplotypes on the left specificity (also in relation to worm system has another peculiar feature in arm of I, functioning genotype) and the study of ecological that the number of , rather than as a poison-antidote (peel-1-zeel-1) associations between nematode , limits offspring production (in system, present in some C. elegans and carrier. Such associations may benign lab conditions). Most C. elegans isolates but absent in others. Both be phoretic (transport), necromenic isolates produce a maximum of about allelic combinations co-occur in some (once the host has died, worms feed 200–350 sperm, the range of observed locations and the maintenance of both off the host corpse and associated offspring production in the laboratory. presently requires an explanation. microbes) and possibly commensal The irreversible sperm-to- The population genetic structure or parasitic. While dauer larvae may switch generates a trade-off between of C. elegans is a consequence of actively disperse at a small scale two key life history parameters: specific organismal characteristics, between food patches, long-range offspring number (sperm number) especially selfing, dauer persistence dispersal likely occurs through these versus maturation time (the time point and migration, and use of ephemeral carrier arthropods and gastropods, when the first oocyte can be fertilized). resources. The colonization of a new or even frugivore vertebrates (birds Genetic variation for self-brood size food source by one or a few genetically and mammals, including humans). C. can be found among natural isolates identical dauer larvae can result in elegans dauer larvae are behaviourally of C. elegans, which is presumably locally clonal populations at a small active and their sensory perception and generated by regulatory changes of spatial scale (a few cm3). At a larger behaviour are elaborate. They are able switching. How ecological spatial scale, migration appears to move rapidly, or erect themselves to components correlate with such sufficient for a substantial portion adopt an intriguing waving behaviour variation in reproductive capacity of the (known) genetic diversity of (known as nictation; Figure 1), which remains uninvestigated. the species to be present in areas may facilitate finding a passing carrier. Male of of less than a km2, perhaps due to Relatively little is known about dauer hermaphrodites may increase the transport of dauers by other mechanoreception and olfaction, which offspring production beyond 1000, animals. The role of colonization are potentially involved in seeking out and the larger and more active hazard in structuring C. elegans spatial carriers and sensing cues for dauer male sperm has precedence over distribution is unknown. exit. hermaphrodite sperm. The complex The estimated overall molecular behaviour of males is, diversity in C. elegans is on the order Reproduction: how many sperm? however, partially degenerated in of 10–3 per base-pair — around C. elegans reproduces through self- selfing Caenorhabditis species. 30-fold lower than in the male–female fertile hermaphrodites and facultative For example, because of a species C. remanei. This low overall males. In XX animals, the soma is retrotransposon insertion in the genetic diversity in C. elegans is likely female, but the germ cells initially corresponding muscin structural the result of the combined effects of develop as sperm during the late L4 , males of many wild C. elegans selfing, strong population bottlenecks stage, before irreversibly switching to isolates are unable to synthesize the and selective sweeps, reducing the develop into oocytes. The resulting copulatory plug, a sticky gelatinous long-term effective population size. In adult hermaphrodite is self-fertile but structure that partially hinders comparison to C. elegans, C. briggsae not capable of inseminating other insemination by other males. has a slightly higher genetic diversity animals. About 0.1% of animals in and shows stronger spatial structuring the lab develop as XO males, after Life cycle and population structure around the globe. spontaneous non-disjunction of X How much does C. elegans mate C. elegans population bottlenecks at . Exposing and outcross in the wild? The vast are followed by rapid population re- L4 animals to various environmental majority of individuals isolated expansions. Bottlenecks increase the stressors, such as high temperature or from natural populations are probability of fixation of deleterious ethanol, can increase the proportion hermaphrodites. Moreover, the . Subsequent compensatory of males. Males reproduce through frequency of heterozygous individuals evolution to suppress such negative mating with hermaphrodites. is very low, indicating an estimate mutational effects has been observed This unusual reproductive mode of the short-term outcrossing rate in the lab through study of appears to have evolved repeatedly of approximately 1%. The long-term accumulation lines where, upon in rhabditid nematodes. Most outcrossing rate, estimated from population re-expansion, extragenic Caenorhabditis species reproduce the level of linkage disequilibrium suppressors alleviate the effects through XX females and XO males — between loci, is 100-fold lower. This of deleterious mutations. The the absence of the Y chromosome is an discrepancy among outcrossing rate metapopulation structure of obvious facilitator for the evolution of estimates may be explained by the C. elegans with frequent bottlenecks selfing in the lineages leading to presence of outbreeding depression. and expansions, further influenced C. elegans, C. briggsae and C. sp. 11. Predominantly selfing species, such by probable source-sink dynamics, Particular ecological parameters, most as C. elegans, seem to have overcome are thus critical elements to account prominently an ephemeral habitat and in the past, and for when studying the evolution of its extreme population bottlenecks upon genetic incompatibilities may occur genetic and phenotypic properties. Current Biology Vol 20 No 22 R968

Microbial fauna in intestinal lumen highly heterogeneous across space and time, is still unclear.

Rotten apple environment Microbes: the good and the bad Snail Microbial communities undoubtedly play a crucial part in C. elegans ecology and have shaped many features of its biology. Bacteria and small serve as food FOOD source and also encompass potential pathogens (Figure 2). Given that food quality and quantity have dramatic PATHOGENS influences on overall life history, a VECTORS rather worrisome problem is that we ? still have a very limited idea of the main natural food sources of PREDATORS C. elegans. In the lab, C. elegans readily feeds on a wide range of bacteria and . Cholesterol uptake — essential for steroid synthesis — may occur in the wild in intestinal cells through ingestion of small eukaryotes. Predatory mite How C. elegans navigates through diverse microbial patches, and to what extent it can discriminate between Nematophagous fungi alternative food sources, is difficult to Current Biology evaluate, but its pharyngeal pumping Figure 2. Biotic interactions of C. elegans. does not appear to be very selective. Schematic overview of possible interactions between C. elegans and its food sources, path- C. elegans N2 is able to disrupt E. coli ogens, predators and carriers. Pictures from wild sampling of C. elegans. *C. elegans being OP50 cells in its pharyngeal grinder, slurped up in a spaghetti-like fashion by a predatory mite (Sancassania sp.). and its fast defecation cycle only allows for a short food residence time in the intestine. Live OP50 cells may survive Environmental interactions adaptation to novel and heterogeneous grinding, enter and proliferate in the C. elegans has a broad repertoire of environments; however, we lack any intestinal lumen of old N2 animals. Such features for sensing and coping with insights into the relationship between a phenotype is considered abnormal environmental complexity in its natural chemoreceptor diversity and their by C. elegans lab biologists, yet is the habitat. Out of the 302 in the ecological significance. norm in freshly isolated wild animals, hermaphrodite, 60 ciliated neurons The flexibility that allows which often show intestinal colonization build the primary sensory system C. elegans to endure environmental by live bacteria and possibly fungi, mediating chemical, thermal, or fluctuations is further reinforced by a leading to ‘constipation’ phenotypes mechanic stimuli. Sensory processing complex molecular stress response (Figure 2, top). Characterizing the guides various behaviours, including machinery, apt to counter potentially natural interactions between C. elegans feeding, mating and egg-laying, as harmful agents, including hypoxia, and its microbial community will clearly well as developmental decisions, osmotic stress, heat, cold, toxins, be important in constructing the natural such as dauer formation. Recent acids or diverse pathogens. The history of this organism. studies have characterized pheromone intestine is a major organ involved in Animals freshly isolated from cocktails that drive mating behaviour detoxification of chemicals as well nature frequently show other signs and dauer formation. Information as pathogen resistance (see below). of infections, including bacterial on chemosensory preferences may While many stress responses are films on the , fungal invasion, provide clues about relevant ecological rapidly triggered, such responses can or intracellular microsporidial parameters linked to foraging and also amplify across generations. For infections (Figure 2). Molecular and habitat choice in the wild. In silico example, animals exposed to high salt cellular responses of C. elegans to analysis of the C. elegans genome concentrations for several generations pathogen infection and pathogen- indicates that chemosensation of show a transgenerational increase in released toxins have been studied gustatory and olfactory cues involves osmotic stress resistance, apparently primarily with strains of medically close to a thousand G - due to elevated parental provisioning relevant human pathogens. Several coupled receptors, evolving at fast of glycerol and sugars to developing signalling pathways, including the rates through gene duplications and embryos. Worms further accommodate TGF-ß, insulin, p38 MAP kinase or pseudogenization, with signatures experience and environment in their ERK pathways, have been co-opted of positive selection. Such genes foraging behaviour through sensory in various defence mechanisms, functioning in environmental adaptation or associative . How including particularly the production interactions are therefore prime established lab responses differ from of antimicrobial peptides and candidates for involvement in natural ones, where conditions are , morphological modification, Magazine R969 but also avoidance behaviour. The C. elegans research has been using ecological and evolutionary hypotheses presence of an RNA silencing system the N2 strain as a reference wild type, in controlled settings, complementary (RNA interference) suggests that from which thousands of mutants approaches may include the study C. elegans also encounters viral have been derived and characterized. of individuals in lab microcosms, or pathogens in the wild. Although As for all genetic model organisms, experimental evolution assays to track general response mechanisms C. elegans biology thus captures the evolutionary process in real time, may be activated upon pathogen a very limited range of genetic which have recently been applied for infection, the C. elegans immune variation, here essentially a single the first time inC. elegans. Overall, the response can also be pathogen- genotype. To what extent certain progress to date from the integration specific. A clear future aim is to study biological observations documented of mechanistic and evolutionary microbial pathogens co-occurring for N2 can be extrapolated to other ecological research on C. elegans with particular C. elegans genotypes C. elegans genotypes (and even more illustrates that a more natural model or populations. Such studies may not so to other species) is questionable. organism is also a more powerful one. only shed light on the co-evolution of Recently, it has come to light that N2 host-pathogen interactions, but also indeed differs from most of its natural Further reading help to understand to what extent conspecifics for many phenotypes Barrière, A., and Félix, M.-A. (2005). High local genetic diversity and low outcrossing rate in immune responses are specific. and that the underlying N2 alleles Caenorhabditis elegans natural populations. Curr. may have arisen in the laboratory. For Biol. 15, 1176–1184. Barrière, A., and Félix, M.-A. (2007). Temporal Community ecology example, genes involved in oxygen dynamics and linkage disequilibrium in natural C. elegans shares its natural sensation and behaviour show a C. elegans populations. 176, 999–1011. environment with a diverse unique combination of alleles in N2 Braendle, C., Milloz, J., and Félix, M.-A. (2008). Mechanisms and evolution of environmental community, in particular arthropods, compared to its wild counterparts. responses in Caenorhabditis elegans. Curr. Top. molluscs and other nematodes, These findings are not surprising, Dev. Biol. 80, 171–207. Cutter, A.D., Dey, A., and Murray, R.L. (2009). some of which also feed on microbes given that the N2 isolate has been Evolution of the Caenorhabditis elegans genome. proliferating upon plant decomposition. undergoing adaptation to artificial Mol. Biol. Evol. 26, 1199–1234. Many are potential dispersal vectors lab environments and numerous Harvey, S.C., and Viney, M.E. (2007). Thermal variation reveals natural variation between as well as predators of C. elegans. bottlenecks for years before freezing. isolates of Caenorhabditis elegans. J. Exp. Zool. Frequently co-occurring predators B Mol. Dev. Evol. 308, 409–416. Hodgkin, J., and Doniach, T. (1997). Natural variation include fungi, which, depending on the Conclusions and perspectives and copulatory plug formation in Caenorhabditis species, invade the nematode through Recent research has started to examine elegans. Genetics 146, 149–164. spores attaching to the cuticle or the C. elegans outside its cushy Petri dish, Kiontke, K., and Sudhaus, W. (2006). Ecology of Caenorhabditis species. In Wormbook, January 9, intestine, or use trapping devices that providing a basis for a revised natural 2006; available from: http://www.wormbook.org. immobilize the animal and perforate history. First and foremost, a modern McGrath, P.T., Rockman, M.V., Zimmer, M., Jang, H., Macosko, E.Z., Kruglyak, L., and Bargmann, it (Figure 2). Nematophagous mites, natural history of C. elegans needs to C.I. (2009). Quantitative mapping of a digenic springtails and nematodes are other evaluate the environmental and genetic behavioral trait implicates globin variation in potential predators often encountered context dependence of organismal C. elegans sensory behaviors. 61, 692–699. Rockman, M.V., and Kruglyak, L. (2009). in the C. elegans habitat. phenotypes by exploring natural Recombinational landscape and population The broader nematode community variational properties of genotype, of Caenorhabditis elegans. PLoS Genet. 5, e1000419. associated with C. elegans comprises environment and phenotypes and their Seidel, H.S., Rockman, M.V., and Kruglyak, L. (2008). microbivorous nematodes, often interrelationships. A very relevant and Widespread genetic incompatibility in C. elegans including other rhabditid nematodes, now feasible approach to shed light on maintained by balancing selection. Science 319, 589-594. such as Oscheius sp., diplogastrids or evolutionarily and ecologically relevant Schulte, R.D., Makus, C., Hasert, B., Michiels, N.K., panagrolaims, which likely compete phenotypes is the fine-scale mapping and Schulenburg, H. (2010). Multiple reciprocal adaptations and rapid genetic change upon with C. elegans for microbial food of genetic variation underlying natural experimental coevolution of an animal host and resources. Also found in rotting fruits are phenotypic variation by means of its microbial parasite. Proc. Natl. Acad. Sci. USA fungal-eating and predatory nematodes. recombinant inbred lines or association 107, 7359–7364. Troemel, E.R., Félix, M.-A., Whiteman, N.K., Barrière, Sometimes, C. elegans co-occurs mapping. A., and Ausubel, F.M. (2008). Microsporidia are with other Caenorhabditis species in The most difficult challenge will natural intracellular parasites of the nematode C. elegans. PLoS Biol. 6, e309. the same location or even in the same be to elucidate the so-far elusive Woodruff, G.C., Eke, O., Baird, S.E., Félix, M.-A., few square millimetres of substrate. ecology of C. elegans through and Haag, E.S. (2010). Insights into species Given the rapid proliferation upon food ‘field studies’ involving extensive divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis availability, intraspecific competition for and repeated monitoring of natural nematodes. Genetics, in press. food is probably substantial. populations across ecologically Zhang, Y., Lu, H., and Bargmann, C.I. (2005). Pathogenic bacteria induce aversive olfactory distinct and well-defined habitats. learning in Caenorhabditis elegans. Nature 438, The unnatural history of C. elegans Population samples can be easily 179–184. research analyzed within a few hours after In the 1960s, chose placing a substrate isolate on a Petri 1Institut Jacques Monod, CNRS - Université C. elegans as an easily cultivable, dish and observing nematodes under Paris-Diderot, 15 rue Hélène Brion, simple metazoan amenable for a dissecting microscope. Yet, there 75205 Paris cedex 13, France. 2 genetic dissection of development, will remain obvious limitations to Institute of Developmental Biology and Cancer, CNRS - University of Nice, Parc neurobiology and behaviour. The meaningful observations on a one Valrose, Bâtiment des Sciences Naturelles, originally used strain, N2, was isolated millimetre long animal in spatially 06108 NICE cedex 2, France. from mushroom farm compost in the and temporally highly heterogeneous E-mail: [email protected]; 1950s in Bristol, UK. Nearly all of environments. To test specific [email protected]