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WIREs Dev Biol
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Nematode model systems in evolution and development

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Abstract The free‐living nematode Caenorhabditis elegans is one of the most important model organisms in all areas of modern biology. Using the knowledge about C. elegans as a baseline, nematodes are now intensively studied in evolution and development. Evolutionary developmental biology or for short, ‘evo‐devo’ has been developed as a new research discipline during the last two decades to investigate how changes in developmental processes and mechanisms result in the modification of morphological structures and phenotypic novelty. In this article, we review the concepts that make nematode evo‐devo a successful approach to evolutionary biology. We introduce selected model systems for nematode evo‐devo and provide a detailed discussion of four selected case studies. The most striking finding of nematode evo‐devo is the magnitude of developmental variation in the context of a conserved body plan. Detailed investigation of early embryogenesis, gonad formation, vulva development, and sex determination revealed that molecular mechanisms evolve rapidly, often in the context of a conserved body plan. These studies highlight the importance of developmental systems drift and neutrality in evolution. WIREs Dev Biol 2012, 1:389–400. doi: 10.1002/wdev.33 This article is categorized under: Comparative Development and Evolution > Model Systems Comparative Development and Evolution > Regulation of Organ Diversity Comparative Development and Evolution > Evolutionary Novelties

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Evolution of vulva induction. (a) While the Caenorhabditis elegans vulva is induced by a one‐step induction from the gonadal anchor cell (AC), other species rely on a two‐step or multi‐step induction. Species that form their vulvae in the posterior body region, including Teratorhabditis, do not rely on an induction by the gonad. (b,c) Genetic and molecular studies have identified that the differences between the one‐step induction of C. elegans and the multi‐step induction of Pristionchus pacificus involves a shift in signaling pathways. While C. elegans vulva formation is induced by epidermal‐growth factor (EGF)/Ras/MAP kinase signaling, P. pacificus vulva induction depends on Wnt signaling involving Wnt ligands expressed in the gonad, such as Ppa‐lin‐44 (b) and Ppa‐mom‐2 and Ppa‐egl‐20, which is expressed in the posterior body region (c).

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Vulva development of Caenorhabditis elegans. The mid‐body Pn.p cells P(3–8).p are set aside for vulva formation by regulatory input from the Hox gene lin‐39. Other Pn.p cells fuse in the L1 stage. P(3–8).p can adopt one of three alternative fates. P6.p adopts the inner vulval fate (1°, black oval), P(5,7).p the outer vulval fate (2°, gray ovals), and P(3,4,8).p a non‐vulval fate (3°, white ovals). This spatial pattern of cell fates relies on an induction of vulval fates by the anchor cell (AC, green oval) of the gonad through epidermal‐growth factor (EGF)/Ras/MAP kinase signaling (green arrows), and lateral signaling between P6.p and its neighbors through a Delta‐Notch pathway (black arrows), which inhibits the 1° fate and activates the 2° fate in P(5,7).p. Each fate corresponds to a specific cell division pattern that is executed in the late L3 stage. The 3° Pn.p cells (dotted) undergo one division and fusion to an epidermal syncytium (s). The 2° Pn.p lineage results in seven progeny, the 1° fate lineage in eight progeny, with characteristic orientations of the third round of division: T, transverse division (left–right); L, longitudinal (anteroposterior division); and U, undivided. In the L4 stage, the symmetric cells of the P5.p and P7.p lineages, and of the two daughters of P6.p, migrate toward each other, fuse and form seven superposed syncytial rings around a vulval invagination. The two sisters of the B granddaughter form two rings, vulB1 and vulB2; the progeny of all other granddaughters forms a single ring. (Reprinted with permission from Ref 14. Copyright 2007 Cell Press)

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Schematic representation of nematode gonads. Cell linage and gonad development of (a) Caenorhabditis elegans hemaphrodites, (b) Panagrellus redivivus females, (c) Mesorhabditis sp. 1179 females, and (d) C. elegans males. Lineages: line length represents the relative timing of divisions. Terminal Xs at the linage base represent cell deaths; black circles represent the distal tip cell (DTC) and white circles represent all other fates. Mesorhaditis starts with a three‐cell primordium as a single germline precursor is present, all others start with a four‐cell primordium with Z(1,4) as precursor of the somatic gonad (red circles) and Z(2,3) as precursor of the germ line (blue circles). Lower pictures show final anatomy of the gonad. C. elegans hermaphrodites have a didelphic gonad, all others a monodelphic gonad. Arrowheads represent the position of the vulva in hermaphrodites/females and the cloaca. (e) The gonadal arms of Pristionchus pacificus hermaphrodites have a novel ventral arm extension in comparison to C. elegans. Line diagrams indicate the path of hermaphrodite gonadal arm extension, the solid dot the position of the vulva. The ventral gonadal arm extension is unique to the Diplogastridae. Light gray shading indicates the Rhabditidae family. Medium gray shading indicates the Diplogastridae family. (Reprinted with permission from Refs 40 and 41. Copyright 2005 Elsevier Ltd.)

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Somatic sex determination in Caenorhabditis elegans. Genetic model for sex determination in hermaphrodites (a) and males (b). A series of negative regulatory interactions triggered by the X:A ratio results in high TRA‐1 activity in hermaphrodites and low TRA‐1 activity in males. TRA‐1 regulates transcription of various sex‐specific genes, such as egg‐laying defective 1 (egl‐1) and male abnormal 3 (mab‐3). C. elegans sex determination genes have distinct phenotypes: tra, transformer of XX animals into males; fem, feminization of XX and XO animals; her, hermaphrodization of XO animals.

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Phylogenetic relationship of rhabditid nematodes. This hypothesis is based on concatenated sequences of the genes for SSU and LSU rRNA and the largest subunit of RNA polymerase II. Six different weighted maximum parsimony jackknife analyses were performed. (Reprinted with permission from Ref 14. Copyright 2007 Cell Press)

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Caenorhabditis elegans early cleavage pattern and variation in gastrulation. (a) C. elegans four‐cell stage with founder cell separation. ABa and Abp form most of the neuronal and epidermal tissue. EMS is a founder cell that divides to give rise to E, the precursor of the gut and MS, a cell that contributes to most of the musculature of the worm. The posterior cell P2 among others will form the germline precursor cells. (b) C. elegans 24‐cell stage. The two founder cells E of the gut have moved into the interior of the embryo. (c) Enoplus brevis 16‐cell stage. The two‐gut precursor cells E have started to migrate inward. (d) Tobrilus diversipapillatus has formed a blastocoel (bc) and after the 64‐cell stage the gut precursor cells migrate into the bc. Source: (a) Schierenberg,58 University of Cologne.

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