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WIREs Dev Biol
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The development of sexual dimorphism: studies of the Caenorhabditis elegans male

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Studies of the development of the Caenorhabditis elegans male have been carried out with the aim of understanding the basis of sexual dimorphism. Postembryonic development of the two C. elegans sexes differs extensively. Development along either the hermaphrodite or male pathway is specified initially by the X to autosome ratio. The regulatory events initiated by this ratio include a male‐determining paracrine intercellular signal. Expression of this signal leads to different consequences in three regions of the body: the nongonadal soma, the somatic parts of the gonad, and the germ line. In the nongonadal soma, activity of the key Zn‐finger transcription factor TRA‐1 determines hermaphrodite development; in its absence, the male pathway is followed. Only a few genes directly regulated by TRA‐1 are currently known, including members of the evolutionarily conserved, male‐determining DM domain Zn‐finger transcription factors. In the somatic parts of the gonad and germ line, absence of TRA‐1 activity is not sufficient for full expression of the male pathway. Several additional transcription factors involved have been identified. In the germ line, regulatory genes for sperm development that act at the level of RNA in the cytoplasm play a prominent role. WIREs Dev Biol 2014, 3:239–262. doi: 10.1002/wdev.136 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Sex Determination Invertebrate Organogenesis > Worms
The five classes of postembryonic blast cells in the L1 larva. The bilateral rows of nine hypodermal seam cells (H0, H1, V1–V6, T) give new hypodermal cells and a sensory structure, the postdeirid; in the male, also the rays. The single row of ventral P cells (P1–P12) give rise to sex‐specific motor neurons as well as sexual structures—the vulva in the hermaphrodite, the hook in the male. Hypodermal B, Y, U, and F divide only in the male, giving many sex‐specific structures and neurons, including spicules, gubernaculum, and proctodeal chamber. The mesoblast cell M gives body wall muscles and sex‐specific muscles in both sexes. Z1 and Z4 generate the somatic structures of the gonad; Z2 and Z3 are the primordial germ cells. (Source: http://www.wormatlas.org)
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Examples of sexual dimorphism of shared neurons in the preanal ganglion. (a) PDB. I. PDB is a motor neuron with cell body in the preanal ganglion and a process that runs around to the dorsal side and makes neuromuscular junctions with dorsal body wall muscles. II. In the hermaphrodite preanal ganglion, PDB makes a small number of gap junctions with other neurons. III. In the male, the anterior process from the cell body is extensively grown out and branched. IV. The male‐specific branches synaptically interact with other neurons in the male mating circuits. PDB is likely to be involved in controlling the ventrally‐arched posture of the male posterior region during mating. (b) LUA. In the hermaphrodite, the LUA interneuron likely functions in the posterior touch circuit, as it connects the PLM touch neuron to the locomotion command interneurons AVA, AVD, and PVC (Chalfie et al., 1985). In the male, LUA plays a similar role mediating connectivity between male‐specific sensory neurons and interneurons (see Ref ).
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Morphogenesis of the male tail during L4. This medial section shows the movement of the nuclei of the tail tip hypodermal cells as the cells fuse and move anteriorly. At the same time the rays extend in the acellular fan (a fold in the outer cuticle), the rectal epithelium forms the proctodeal chamber and spicules, and the extending vas deferens connects to the proctodeum. Elongation of the spicules requires their muscle attachments, whereas general retraction of the body is driven in part by pressure in the liquid‐filled space that increasingly separates the nascent adult cuticle from the overlying L4 cuticle (S.W.E unpublished). (Source: http://www.wormatlas.org)
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Four cases where regulatory transcription factors specifying male differentiation have been identified. Transcription of these genes is repressed in hermaphrodites by TRA‐1 DNA binding upstream (mab‐3, dmd‐3), downstream (egl‐1), or within an intron (ceh‐30).
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Events in sex determination differ in three parts of the body: the soma apart from the gonad, the somatic parts of the gonad, and the germ line. In each region, HER‐1 binding to the TRA‐2 receptor dictates male fate. In the somatic body, this results in elimination of the activity of the female‐pathway determining Zn‐finger transcription factor TRA‐1 by the ubiquitin pathway fem genes. In XX individuals, TRA‐2 inhibits the FEM proteins. In addition, an unknown signal possibly independent of the HER‐1/TRA‐2/fem pathway promotes some TRA‐1 activity (the dotted line). In the somatic parts of the gonad, similar events occur, but TRA‐1 retains some activity in the male and additional transcription factors contribute to male versus hermaphrodite pathways. In the germ line, two cytoplasmic proteins, FOG‐1 and FOG‐3, are essential for sperm differentiation and require the FEM proteins for their activity. In the adult male, TRA‐1 promotes FOG‐1 and FOG‐3 activity for continued sperm production. For further details of these pathways, see text.
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The two adult sexual forms of Caenorhabditis elegans, hermaphrodite (top) and male. The male body is smaller and thinner, has specialized copulatory structures in the tail with male‐specific muscles that control them, and expresses sex‐specific behaviors, most notably copulation. The hermaphrodite gonad has two U‐shaped, reflexed arms, arrayed symmetrically about the central vulva, whereas the single‐armed male gonad opens at the cloaca. In both sexes, germ line stem cells reside in the distal gonad. In the hermaphrodite, mature oocytes in the proximal gonad are fertilized as they pass through the spermatheca and embryos begin to develop in the uterus. In the male, sperm mature in the proximal gonad, and are stored in the seminal vesicle before ejaculation in fluids generated by the vas deferens. Bottom two images: the male tail is specialized for copulation. Left: Nomarski image, ventral view, showing the five types of sensilla. The fan is an acellular fold of the outer layer of the cuticle. Right: Scanning EM, ventral view. The spicules, structures that are inserted into the hermaphrodite vulva during mating, can be seen protruding from the cloaca. (Source: http://www.wormatlas.org)
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Differentiation of amoeboid sperm from germ cells. Most of the cytoplasmic contents are left in a residual body as four spermatids are produced. (Reprinted with permission from Ref . Copyright 1981 Rockefeller University Press)
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The posterior ganglia are much enlarged in the male, due to an additional 81 male‐specific neurons. The 89 neurons present in the bilateral lumbar and single dorso‐rectal and pre‐anal ganglia in the hermaphrodite are also present in the male. The lumbar ganglia are enlarged mainly by the addition of 18 ray neurons and 9 ray support cells on each side, while the remaining male‐specific neurons populate the other two ganglia plus a bilateral pair of cloacal ganglia. CG(L/R), cloacal ganglia; DRG, dorsorectal ganglion; LG(R/L), lumbar ganglia; PAG, pre‐anal ganglion; VNC, ventral nerve cord; DNC, dorsal nerve cord. (Source: http://www.wormatlas.org)
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The steps of male mating. When a competent, well‐fed adult male encounters a hermaphrodite, it responds by scanning its tail along the hermaphrodite body in order to locate the vulva. Scanning continues on both sides of the body until this is achieved. At the vulva, it prods with its spicules. When the spicules breach the vulval opening, prodding ceases and the spicules remain protracted while seminal fluid passes into the uterus. Finally, the male retracts its spicules and swims away. This stereotyped program is flexible. Steps can be skipped over or the program backed up as appropriate to achieve the final goal. (Reprinted with permission from Ref . Copyright 2012 AAAS)
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Allocation of cell fates by cell–cell interactions in the cell lineages leading to development of the male hindgut structures. (a and b) Several of the fates of intermediate cells in the B lineage branches generated by a left/right divisionare specified by final cell position rather than lineage ancestory. (c) Arrangement of the cells as the lineage proceeds. Some of the cells in left right branches migrate to the midline, where their fates are set by signals with neighbors. Their order along the a/p axis is not predetermined, leading to the indeterminancy mentioned above. (Source: http://www.wormatlas.org). (Reprinted with permission from Ref . Copyright 1993 The Company of Biologists Limited)
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The muscles of the male tail (left side for left/right pairs, denoted by ‘L’): dBWM, dorsal body wall muscle; vBWM, ventral body wall muscle; aol, anterior outer longitudinal; pol, posterior outer longitudinal; cdl, caudal longitudinal; dgl, diagonal; grt, gubernacular retractor; gec, gubernacular erector; aob, anterior oblique; pob, posterior oblique; v/dsr, ventral/dorsal spicule retractor; v/dsp, ventral/dorsal spicule protractor; adp, anal depressor; ail, anterior inner longitudinal; pil, posterior inner longitudinal. Bottom two diagrams: the sex shared sphincter (sph) and anal depressor (adp) muscles reorient in the adult male. (Source: http://www.wormatlas.org)
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Sex‐specific cells generated by the P‐cell lineages. CA and CP neurons innervate the gonad and body wall muscles, as well as each other and additional neurons; VC neurons innervate vulval muscles. While the details are different, note the similarities: in both sexes the anterior P‐cell daughters generate neurons that control the genital structures, while more posterior daughters generate hypodermal cells that differentiate the genital opening.
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The postembryonic cell lineages leading to the rays. Each ray has a unique identity affecting morphogenesis, neurotransmitter and neuropeptide expression. The identities of rays 1–6 are defined by expression of the Hox genes mab‐5 and egl‐5. In the absence of EGL‐5, mab‐5 expression is not selectively turned off and all the V6 rays take the identity of ray 2.
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