Overview

Brief Summary

Caenorhabditis elegans is a small (~1mm long) nematode worm (roundworm) in the family Rhabditidae. It is cosmopolitan in distribution, with reproductive stages found most reliably in rotting fruits and surrounding soil. When food is plentiful, a fertilized egg completes embryogenesis, passes through four larval stages, and attains reproductive maturity in only three days at room temperature. As with most terrestrial nematodes, under stressful conditions an alternative third larval stage specialized for dispersal, the dauer larva, may be formed. In soil, C. elegans is often found in the dauer form. The reproductive mode of C. elegans involves a mixture of self-fertile hermaphrodites and males (this system was derived relatively recently from an ancestral male/female system). The transparency, anatomical simplicity, rapid development, and mix of outcrossing and selfing in C. elegans led American nematologist Ellsworth Dougherty and British molecular geneticist Sydney Brenner to champion this species as a model organism for basic biological research beginning in the 1970s. By the early 1980's, Brenner and colleagues had carried out pioneering studies investigating the invariant cell lineages, neuroanatomy, and aspects of the genome of C. elegans. This rich body of work garnered the attention of many more researchers and quickly led to C. elegans becoming one of the most widely studied laboratory organisms in the fields of genetics, cell biology, development, aging, evolution, and neuroscience. In 1998, C. elegans became the first animal to have its entire genome sequence determined and it remains at the forefront of functional genomics.

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Distribution

Geographic Range

Caenorhabditis elegans live in temperate regions in many parts of the world (Nicholas 1975).

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Physical Description

Morphology

Physical Description

Caenorhabditis elegans have elongated cylindrical bodies, tapered at both ends, with smooth skin, no segmentation, and no appendages. Adults grow to approximately 1mm in length. Exactly 959 cells compose Caenorhabditis elegans, and their bodies are transparent; therefore, individual cells are easily observed with a microscope (Edgley 1999).

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Ecology

Habitat

Caenorhabditis elegans are terrestrial organisms. They live primarily in soil (Lee & Atkinson 1977). The soil must have a constant level of moisture, so that the worm can move in the film of water and draw water from the soil. The soil must also have a moderate oxygen content. Worms may not be able to penetrate soils with high clay content. For ideal movement, the worm should be about three times as long as the diameter of the soil particles ( Nicholas 1975). Worms are also found in or on rotting vegetation above ground (Edgley 1999).

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Trophic Strategy

Food Habits

Caenorhabditis elegans are bacteriovorous; they feed on various types of bacteria that live in soil and on rotting vegetation. They feed by ingesting bacteria in suspension or on detritus (Nicholas 1975).

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Life History and Behavior

Life Expectancy

Lifespan/Longevity

Average lifespan

Status: captivity:
0.16 years.

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Lifespan, longevity, and ageing

Maximum longevity: 0.16 years (captivity) Observations: These animals are free-living nematodes usually found in the soil of temperate environments. Temperature influences the lifespan of the roundworm with higher temperatures shortening lifespan and lower temperatures extending lifespan, at least until a certain threshold (Klass 1977). Several genetic manipulations have succeeded in extending the longevity of the roundworm, but many of these take into account the dauer stage, which involves a developmental arrest (Klass and Hirsh 1976). As such, the maximum longevity is a conservative estimate. Although physiological ageing has been described in roundworms, the cause of death of old animals remains a mystery.
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Reproduction

Caenorhabditis elegans have two naturally occurring sexes, a male and a self-fertilizing hermaphrodite; females do not naturally occur. The majority of individuals are hermaphrodites; males usually comprise no more than 0.20% of the natural population. The number of males can be increased, however, by raising the temperature at the onset of sexual maturity (Nicholas 1975). Hermaphrodites are protandrous; the individuals produce sperm first and then produce eggs (Blaxter 1999). Most commonly, worms will simply fertilize their own eggs (Bird 1991). However, the males that do exist copulate with hermaphrodites, thus mixing up the gene pool in the population (Nicholas 1975). Eggs are laid within two to three hours of fertilization and hatch approximately twelve hours later. The worms develop into adults in four larval stages; this generally takes about three days when the temperature ranges from 20 to 25 degrees Celsius (Blaxter 1999). Temperature plays a major role in the development of Caenorhabditis elegans. The worms' average lifespan is two to three weeks (Edgley 1999).

Images of Caenorhabditis elegans and sperm:   http://www.mcb.arizona.edu/Wardlab/gallery.html (Muhlrad 1998)

Average age at sexual or reproductive maturity (male)

Sex: male:
3 days.

Average age at sexual or reproductive maturity (female)

Sex: female:
3 days.

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Molecular Biology and Genetics

Molecular Biology

Barcode data: Caenorhabditis elegans

The following is a representative barcode sequence, the centroid of all available sequences for this species.


There are 18 barcode sequences available from BOLD and GenBank.  Below is a sequence of the barcode region Cytochrome oxidase subunit 1 (COI or COX1) from a member of the species.  See the BOLD taxonomy browser for more complete information about this specimen and other sequences.

GCAGTTTGATTAGAGAGATCTAATCATAAAGATATCGGAACTCTTTATTTTATTTTTGGACTTTGATCTGGTATAGTTGGTACTAGATTT---TCTTTATTAATTCGTTTAGAATTAGCTAAACCAGGTTTTTTTCTTAGGAAT---GGACAGTTATATAATTCAGTTATTACAGCTCATGCAATTTTAATAATTTTTTTTATGGTAATACCTACTATAATCGGTGGTTTTGGTAATTGATTATTACCACTTATG---TTAGGAGCACCCGATATAAGATTTCCACGTTTAAATAATTTAAGATTTTGATTATTACCTACATCTATATTATTAATTTTAGATGCTTGTTTTGTAGATATAGGTTGTGGGACTAGGTGAACAGTCTACCCACCTTTAAGA---ACAATGGGGCACCCCGGAAGTAGAGTAGATTTA---GCTATTTTTAGTTTACATGCAGCAGGGTTAAGATCTATTTTAGGTGGTATTAATTTTATGTGTACTACTAAAAATTTACGTAGAAGTTCTATTTCATTAGAACATATAACTTTATTTGTTTGAACTGTGTTTGTAACAGTGTTTTTATTGGTTTTATCTCTACCGGTTTTAGCAGGG---GCTATTACTATGTTGTTAACTGATCGTAATTTAAATACTTCATTTTTTGATCCAAGAACTGGAGGTAATCCTCTTATTTATCAACATTTATTTTGATTTTTTGGTCATCCTGAAGTATATATTTTGATTTTACCAGCTTTTGGTATTGTTAGACAATCTACACTTTATTTAACAGGAAAAAAA---GAAGTTTTTGGTGCTTTGGGTATGGTTTATGCAATTTTAAGAATTGGTTTAATTGGTTGTGTAGTATGAGCTCACCACATGTATACAGTCGGTATAGATTTGGATTCACGTGCTTATTTTTCGGCGGCTACTATGGTTATTGCAGTGCCTACAGGTGTTAAAGTGTTTAGATGATTG---GCTACA
-- end --

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Statistics of barcoding coverage: Caenorhabditis elegans

Barcode of Life Data Systems (BOLDS) Stats
Public Records: 18
Specimens with Barcodes: 18
Species With Barcodes: 1
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Conservation

Conservation Status

Caenorhabditis elegans are not endangered or threatened; they are found in large numbers in nature.

US Federal List: no special status

CITES: no special status

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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Negative

This species has no known negative impact on humans.

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Economic Importance for Humans: Positive

Caenorhabditis elegans are used often in scientific research; they are considered a model organism and are easy to study due to their transparency. They are bred for use as laboratory specimens.

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Wikipedia

Caenorhabditis elegans

Caenorhabditis elegans /ˌsnɵræbˈdɪtɪs ˈɛlɛɡænz/ is a free-living (non-parasitic), transparent nematode (roundworm), about 1 mm in length,[2] that lives in temperate soil environments. The name is a blend of Greek (caeno- - recent, rhabditis - rod-like)[3] and Latin (elegans - elegant). In 1900, Maupas initially named it Rhabditides elegans, Osche placed it in the subgenus Caenorhabditis in 1952, and in 1955, Dougherty raised it to the status of genus.[4]

C. elegans is an unsegmented pseudocoelomate, and lacks a respiratory and a circulatory system. The majority of these nematodes are female hermaphrodites. Males have specialised tails for mating that include spicules. They possess gut granules which emit a brilliant blue fluorescence and a wave of this is seen at death in a death fluorescence.

In 1974, Sydney Brenner began research into the molecular and developmental biology of C. elegans, which has since been extensively used as a model organism.[5]

C. elegans was the first multicellular organism to have its whole genome sequenced. And as of 2012, this worm was the only organism to have its connectome (neuronal "wiring diagram") completed.[6]

Anatomy[edit]

Movement of wild-type C. elegans

C. elegans is unsegmented, vermiform, and bilaterally symmetrical. It has a cuticle, four main epidermal cords, and a fluid-filled pseudocoelom, (body cavity). They also have some of the same organ systems as larger animals. Almost all individuals of C. elegans are female hermaphrodites; and there is a small minority of, around one in a thousand, true males.[7] The basic anatomy of C. elegans includes a mouth, pharynx, intestine, gonad, and collagenous cuticle. Like all nematodes they have neither a circulatory nor a respiratory system. The four bands of muscles that run the length of the body are connected to a neural system that allows the muscles to move the animal's body only in the dorsal/ventral direction; hence, any living, moving individual is always on either its left or its right side when observed crossing a horizontal surface.

Males have a single-lobed gonad, a vas deferens, and a tail specialized for mating, which incorporates spicules. Hermaphrodites have two ovaries, oviducts, spermatheca, and a single uterus.

Microanatomy[edit]

There are numerous gut granules present in the intestine of C. elegans, the functions of which are still not fully known, as are many other aspects of this nematode, despite the many years that it has been studied. These gut granules are found in all of the Rhabdita orders. They are very similar to lysosomes in that they feature an acidic interior and the capacity for endocytosis, but they are considerably larger, reinforcing the view of their being a storage organelle. A remarkable feature of the granules is that when they are looked at under ultraviolet light, they react by emitting an intense blue fluorescence. Another phenomenon seen is termed death fluorescence. As the worms die, a dramatic burst of blue fluorescence is emitted. This death fluorescence typically takes place in an anterior to posterior wave that moves along the intestine, and is seen in both young and old worms, subjected to lethal injury or peacefully dying of old age. There have been many theories on the functions of the gut granules with earlier ones being eliminated by later findings. It is thought that they store zinc as one of their functions. Recent chemical analysis has identified the blue fluorescent material that they contain as a glycosylated form of anthranilic acid (AA). The need for the large amounts of AA that the many gut granules contain is questioned. One possibility is that the AA is anti-bacterial and used in defense of invading pathogens. Another possibility, is that the granules provide photoprotection: the bursts of AA fluorescence entails the conversion of damaging UV light to relatively harmless visible light. There is seen a possible link here to the melanin–containing melanosomes.[8]

Reproduction and development[edit]

Anatomical diagram of a male C. elegans

The hermaphrodite, which is considered to be a specialized form of self-fertile female because its soma is female whereas its germ line produces male gametes first, lays eggs through its uterus after internal fertilization. Under environmental conditions which are favourable for reproduction, hatched larvae develop through 4 stages or molts, designated as (L1 to L4). When conditions are stressed as in food insufficiency, C. elegans can enter an alternative third larval stage called the dauer state. Dauer is German for permanent. Dauer larvae are stress-resistant; they are thin and their mouths are sealed and cannot take in food and they can remain in this stage for a few months.[9] Hermaphrodites produce all their sperm in the L4 stage (150 sperm per gonadal arm) and then produce only oocytes. The sperm are stored in the same area of the gonad as the oocytes until the first oocyte pushes the sperm into the spermatheca (a chamber wherein the oocytes become fertilized by the sperm).[10] The male can inseminate the hermaphrodite, which will preferentially use male sperm (both types of sperm are stored in the spermatheca). When self-inseminated, the wild-type worm will lay approximately 300 eggs. When inseminated by a male, the number of progeny can exceed 1,000. At 20 °C, the laboratory strain of C. elegans has an average life span of approximately two–three weeks and a generation time of approximately four days.

Nematodes have a fixed, genetically determined number of cells, a phenomenon known as eutely. The male C. elegans for example has 1031 cells, a number which does not change after cell division ceases at the end of the larval period. Growth is solely due to an increase in the size of individual cells.[11]

A lateral (left) side anatomical diagram of an adult-stage C. elegans hermaphrodite

Ecology[edit]

The different Caenorhabditis species occupy various nutrient and bacteria rich environments. They feed on the bacteria that develop in decaying organic matter. Soil lacks enough organic matter to support self-sustaining populations. C. elegans can survive on a diet of a variety of many kinds of bacteria, but its wild ecology is largely unknown. Most laboratory strains were taken from artificial environments such as gardens and compost piles. More recently, C. elegans has been found to be thriving in other kinds of organic matter, particularly rotting fruit.[12] Invertebrates such as millipedes, insects, isopods, and gastropods can transport dauer larvae, to various suitable locations. The larvae have also been seen to feed on their host when it dies.[13]

Nematodes can survive desiccation, and in C. elegans the mechanism for this capability has been demonstrated to be late embryogenesis abundant (LEA) proteins.[14]

Research use[edit]

Asymmetric cell divisions during early embryogenesis of C. elegans.

In 1963, Sydney Brenner proposed using C. elegans as a model organism for the investigation primarily of neural development in animals. It is one of the simplest organisms with a nervous system. In the hermaphrodite, this system comprises 302 neurons[15] the pattern of which has been comprehensively mapped, in what is known as a connectome, and shown to be a small-world network.[16] Research has explored the neural mechanisms that control several behaviors of C. elegans, including chemotaxis, thermotaxis, mechanotransduction, and mating behaviour.[17] Brenner also chose it as it is easy to grow in bulk populations, and convenient for genetic analysis.[18] It is a multicellular eukaryotic organism that is simple enough to be studied in great detail. Strains are cheap to breed and can be frozen. When subsequently thawed, they remain viable, allowing long-term storage.[19]

Notable findings[edit]

The transparency of C. elegans facilitates studying cellular differentiation and other developmental processes in the intact organism. The morphology of the tail region with its spicules, clearly distinguishes males from hermaphrodites.

The developmental fate of every single somatic cell (959 in the adult hermaphrodite; 1031 in the adult male) has been mapped.[20][21] These patterns of cell lineage are largely invariant between individuals, whereas in mammals, cell development is more dependent on cellular cues from the embryo..

The first cell divisions of early embryogenesis in C. elegans are among the best understood examples of asymmetric cell divisions.[22]

Programmed cell death (apoptosis) eliminates many additional cells (131 in the hermaphrodite, most of which would otherwise become neurons); this "apoptotic predictability" has contributed to the elucidation of some apoptotic genes, mainly through observation of abnormal, apoptosis-surviving nematodes.

Wild-type C. elegans hermaphrodite stained with the fluorescent dye Texas Red to highlight the nuclei of all cells

RNA interference (RNAi) is a relatively straightforward method of disrupting the function of specific genes. Silencing the function of a gene can sometimes allow a researcher to infer its possible function(s). The nematode can be either soaked in or injected with a solution of double-stranded RNA, the sequence of which complements the sequence of the gene that the researcher wishes to disable; worms can alternatively be fed genetically transformed bacteria that express the double-stranded RNA of interest. Gene loss-of-function experiments in C. elegans are the easiest of all animal models, enabling scientists to establish that approximately 10% of the 20,000 genes in its genome are 'essential', meaning that RNAi knockdown of those genes resulted in "sterility, embryonic or larval lethality, slow post-embryonic growth, or a post-embryonic defect."[23]

Environmental RNAi uptake is much worse in other species of worm in the Caenorhabditis genus. Although injecting RNA into the body cavity of the animal induces gene silencing in most species, only C. elegans and a few other distantly related nematodes can uptake RNA from the bacteria that they eat for RNAi.[24] This ability has been mapped down to a single gene, sid-2, which, when inserted as a transgene in other species, allows them to so uptake RNA for RNAi as C. elegans does.[25]

Studying meiosis is considerably simplified. As sperm and egg nuclei move down the gonad, so they temporally progress through meiotic events; the difficulties of heterogenous cellular populations are eliminated because every nucleus at a given position in the gonad therefore is at roughly the same step in meiosis. Research (2013) has shown that in a very early phase of meiosis the oocytes formed are extremely resistant to radiation.[26][27]This resistance is seen to be due to the expression of a single gene which has been seen to efficiently repair any such DNA damage caused. The identified protein for this is MRE11A.[28] A study of the frequency of outcrossing in natural populations showed that selfing is the predominant mode of reproduction in C. elegans, but that infrequent outcrossing events occur at a rate of approximately 1%.[29] Meioses that result in selfing are unlikely to contribute significantly to beneficial genetic variability, but these meioses may provide the adaptive benefit of recombinational repair of DNA damages that arise, especially under stressful conditions.[30]

It can also be used to study nicotine dependence because it exhibits behavioral responses to nicotine that parallel those of mammals; e.g., acute response, tolerance, withdrawal, and sensitization.[31]

As for most model organisms, scientists that work in the field curate a dedicated online database and the WormBase is that for C. elegans. The WormBase attempts to collate all published information on C. elegans and other related nematodes. Their website has advertised a reward of $4000 for the finder of a new species of closely related nematode.[32] Such a discovery would broaden research opportunities with the worm.[33]

C. elegans has been a model organism for research into ageing; for example - the inhibition of an insulin-like growth factor, signaling pathway has been shown to increase adult lifespan threefold.[34] Moreover, extensive research on C. elegans has identified RNA-binding proteins as essential factors during germline and early embryonic development.

C. elegans has five pairs of autosomes and one pair of sex chromosomes. Sex in C. elegans is based on an X0 sex-determination system. Hermaphrodite C. elegans have a matched pair of sex chromosomes (XX); the rare males have only one sex chromosome (X0). The sperm of C. elegans is ameboid, lacking flagella and acrosomes.

C. elegans is notable in animal sleep studies as the most primitive organism to display sleep-like states. In C. elegans, a lethargus phase occurs shortly before each moult.

Spaceflight research[edit]

C. elegans made news when specimens were discovered to have survived the Space Shuttle Columbia disaster in February 2003.[35] Later, in January 2009, live samples of C. elegans from the University of Nottingham were announced to be spending two weeks on the International Space Station that October in a project to explore the effects of zero gravity on muscle development and physiology. The research was primarily about genetic basis of muscle atrophy, which relates to spaceflight or being bed-ridden, geriatric, or diabetic.[36] Descendants of the worms aboard Columbia in 2003 were launched into space on Endeavour for the STS-134 mission.[37]

Genome[edit]

C. elegans adult with GFP coding sequence inserted into a histone-encoding gene by Cas9-triggered homologous recombination
C. elegans hermaphrodite

C. elegans was the first multicellular organism to have its whole genome sequenced. The sequence was published in 1998[38] although some small gaps were present; the last gap was finished by October 2002. The C. elegans genome is approximately 100 million base pairs long and consists of six chromosomes and a mitochondrial genome. Its gene density is about 1 gene/5kb, (5 kilo-base pairs). Introns, or non-expressed sequences, are 26% of the genome. Some large, intergenic regions contain repetitive DNA sequences. Many genes are arranged in operons, which are polycistronic series that are together transcribed. C. elegans and other nematodes are among the few eukaryotes currently known to have operons; these include trypanosomes, flatworms notably the trematode Schistosoma mansoni, and a primitive chordate tunicate Oikopleura dioica. It is believed that many more organisms will be shown to have these operons.[39]

The genome contains approximately 20,470 protein-coding genes.[40] About 35% of C. elegans genes have human homologs. Remarkably, it has been shown repeatedly that human genes replace their C. elegans homologs when introduced into C. elegans. Conversely, many C. elegans genes can function similarly to mammalian genes.[9] The number of known RNA genes in the genome has increased greatly due to the 2006 discovery of a new class of 21U-RNA genes,[41] and the genome is now believed to contain more than 16,000 RNA genes, up from as few as 1,300 in 2005.[42] Scientific curators continue to appraise the set of known genes: new gene predictions continue to be added and incorrect ones modified or removed.

In 2003, the genome sequence of the related nematode C. briggsae was also determined, allowing researchers to study the comparative genomics of these two organisms.[43] The genome sequences of more nematodes from the same genus e.g., C. remanei,[44] C. japonica[45] and C. brenneri are under study [46] via the whole genome shotgun technique, which is less complete and accurate than the "hierarchical" or clone-by-clone approach that was used on C. elegans.

The official version of the C. elegans genome sequence continues to change as new evidence reveals errors in the original sequencing. Most changes are minor, adding or removing only a few base pairs (bp) of DNA. For example, the WS202 release of WormBase (April 2009) added two base pairs to the genome sequence.[47] More extensive changes are sometimes made; e.g., the WS197 release of December 2008, which added a region of over 4,600 bp to the sequence.[48][49]

Evolution[edit]

A few conserved protein sequences in the distantly related sponges more resemble those of humans than of C. elegans.[50] An accelerated rate of evolution may therefore have occurred in the C. elegans lineage. The same study found that several phylogenetically ancient genes are absent in C. elegans.

Scientific community[edit]

In 2002, the Nobel Prize in Physiology or Medicine was awarded to Sydney Brenner, H. Robert Horvitz and John Sulston for their work on the genetics of organ development and programmed cell death in C. elegans. The 2006 Nobel Prize in Physiology or Medicine was awarded to Andrew Fire and Craig C. Mello for their discovery of RNA interference in C. elegans.[51] In 2008, Martin Chalfie shared a Nobel Prize in Chemistry for his work on green fluorescent protein; some of the research involved the use of C. elegans.

Many scientists who research C. elegans closely connect to Sydney Brenner, with whom almost all research in this field began in the 1970s; they have worked as either a post-doctoral or a post-graduate researcher in Brenner's lab or in the lab of someone who previously worked with Brenner. Most who worked in his lab later established their own worm research labs, thereby creating a fairly well-documented "lineage" of C. elegans scientists, which was recorded into the WormBase database in some detail at the 2003 International Worm Meeting.

See also[edit]

References[edit]

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  2. ^ Wood, WB (1988). The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press. p. 1. ISBN 0-87969-433-5. 
  3. ^ καινός (caenos) = new, recent; ῥάβδος (rhabdos) = rod, wand.
  4. ^ Ferris, H (30 November 2013). "Caenorhabditis elegans". University of California, Davis. Retrieved 2013-11-19. 
  5. ^ Brenner, S (1974). "The Genetics of Caenorhabditis elegans". Genetics 77 (1): 71–94. PMC 1213120. PMID 4366476. 
  6. ^ Jabr, Ferris (2012-10-02). "The Connectome Debate: Is Mapping the Mind of a Worm Worth It?". Scientific American. Retrieved 2014-01-18. 
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  8. ^ Coburn, C; Gems, D (2013). "The mysterious case of the C. Elegans gut granule: Death fluorescence, anthranilic acid and the kynurenine pathway". Frontiers in Genetics 4: 151. doi:10.3389/fgene.2013.00151. PMC 3735983. PMID 23967012. 
  9. ^ a b "Intoduction to C. Elegans". C. Elegans as a model organism. Rutgers University. Retrieved 6 February 2014. 
  10. ^ Nayak, S; Goree, J; Schedl, T (2004). "fog-2 and the Evolution of Self-Fertile Hermaphroditism in Caenorhabditis". PLoS Biology 3 (1): e6. doi:10.1371/journal.pbio.0030006. PMC 539060. PMID 15630478. 
  11. ^ Ruppert, Edward E.; Fox, Richard, S.; Barnes, Robert D. (2004). Invertebrate Zoology, 7th edition. Cengage Learning. p. 753. ISBN 978-81-315-0104-7. 
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  17. ^ Schafer, W.R. Deciphering the neural and molecular mechanisms of C. Elegans behaviour. Curr.Biol.2005.Sep 6.PMID 16139205
  18. ^ Avery, L. "Sydney Brenner". Southwestern Medical Center. [dead link]
  19. ^ Brenner, S (1974). "The Genetics of Caenorhabditis elegans". Genetics 77 (1): 71–94. PMC 1213120. PMID 4366476. 
  20. ^ Sulston, JE; Horvitz, HR (1977). "Post-embryonic cell lineages of the nematode, Caenorhabditis elegans". Developmental Biology 56 (1): 110–56. doi:10.1016/0012-1606(77)90158-0. PMID 838129. 
  21. ^ Kimble, J; Hirsh, D (1979). "The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans". Developmental Biology 70 (2): 396–417. doi:10.1016/0012-1606(79)90035-6. PMID 478167. 
  22. ^ Gönczy, P (2005). "Asymmetric cell division and axis formation in the embryo". WormBook: 1. doi:10.1895/wormbook.1.30.1. 
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