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Comparative Morphology of the Body Wall in Flatworms (Platyhelminthes)1

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Comparative Morphology of the Body Wall in Flatworms (Platyhelminthes)1 194 REVIEW / SYNTHÈSE Comparative morphology of the body wall in flatworms (Platyhelminthes)1 Seth Tyler and Matthew Hooge Abstract: The soft-bodied nature of the platyhelminths is due largely to the structure of the body wall and its lack of sclerotic elements such as cuticle. Free-living members, i.e., most turbellarians, show considerable variety, but the basic form of the body wall comprises a simple ciliated epithelium overlying a network of muscles. We illustrate this body wall structure in a representative typhloplanoid rhabditophoran and discuss variations in representatives of the Acoela, Catenulida, and other free-living rhabditophorans. The major parasitic groups of platyhelminths, the rhabditophoran Neodermata, follow a developmental pattern that replaces a similar ciliated epidermis in a larval stage with a special- ized epidermis called a neodermis, which is assumed to be key to their success as parasites. This neodermis consists of a syncytium that covers the body in a continuous sheet connected to perikarya that lie below the body wall muscula- ture. The neodermis can be seen as a special adaptation of a developmental mechanism common to all platyhelminths, in which epidermal growth and renewal are accomplished by replacement cells originating beneath the body wall. The cell type responsible for all cell renewal, including body wall renewal, in platyhelminths is the neoblast, and its pres- ence may be the one autapomorphic character that unites all taxonomic groups of platyhelminths. Résumé : Le corps mou des plathelminthes s’explique en grande partie par la structure de leur paroi corporelle et l’absence d’éléments sclérotiques, tels que la cuticule. Les groupes libres, c’est-à-dire la majorité des turbellariés, sont très variés, mais la structure de base de leur paroi consiste en un simple épithélium cilié superposé à un réseau de muscles. Nous illustrons cette structure de la paroi chez un rhabditophore typhloplanoïde typique, et nous commentons les variations observées chez des représentants des acoeles, des caténulides et d’autres rhabditophores libres. Le groupe principal de platheminthes parasites, les rhapditophores néodermates, ont une séquence de développement au stade lar- vaire pendant laquelle un épiderme cilié de même type que celui des turbellariés libres est remplacé par le néoderme, un épiderme spécialisé qui assure, croit-on, leur succès comme parasites. Ce néoderme forme un syncytium qui re- couvre le corps en une couche continue qui est rattachée à des péricaryons situés sous la musculature de la paroi. Le néoderme peut être considéré comme une adaptation particulière d’un mécanisme de développement commun à tous les plathelminthes dans lequel la croissance et le renouvellement de l’épiderme s’accomplissent par des cellules de re- change provenant de sous la paroi. Le type cellulaire responsable du renouvellement de toutes les cellules, y compris celles de la paroi, chez les plathelminthes est le néoblaste dont la présence peut être le caractère apomorphe qui unit tous les groupes taxonomiques de plathelminthes. [Traduit par la Rédaction] Tyler and Hooge 210 Introduction The soft-bodied nature arises largely from the relative sim- plicity of the body wall: a simple epithelium (i.e., single lay- Flatworms are soft-bodied bilaterians with a body struc- ered) overlying a network of muscles and lacking cuticle or ture that has inspired some evolutionary biologists to use dermal skeletal elements (Fig. 1). them as models for the ancestor of the rest of the Bilateria. The free-living flatworms, known as turbellarians (class Turbellaria in non-cladistic classifications), have, for the Received 25 February 2003. Accepted 6 August 2003. most part, a ciliated, cellular epidermis (Fig. 1A), whereas Published on the NRC Research Press Web site at the parasitic flatworms, the Neodermata (encompassing the http://cjz.nrc.ca on 16 April 2004. classes Trematoda, Monogenea, and Cestoda), have a syn- S. Tyler2 and M. Hooge. Department of Biological Sciences, cytial, nonciliated epidermis whose nuclei-bearing parts lie University of Maine, 5751 Murray Hall, Orono, ME 04469- sunken below the musculature (Fig. 1B). Turbellarians show 5751, USA. considerable variety, however: special regions of the epider- 1This review is one of a series dealing with aspects of the mis may have a syncytial structure or sunken cell bodies, or biology of the phylum Platyhelminthes. This series is one of may lack cilia. Reflecting their origins from a turbellarian- several virtual symposia on the biology of neglected groups like ancestor, the Neodermata have a larval stage bearing a that will be published in the Journal from time to time. ciliated, cellular epidermis, much like that of turbellarians, 2Corresponding author (e-mail: [email protected]). and this is replaced by the syncytial epidermis, which is then Can. J. Zool. 82: 194–210 (2004) doi: 10.1139/Z03-222 © 2004 NRC Canada Tyler and Hooge 195 Fig. 1. (A) Schematic representation of the body wall and its layering in turbellarian flatworms as seen in a cut-away view of the body. A typical cellular, ciliated epidermis (with cilia drawn on only some cells) and a layering of diagonal muscle fibers between cir- cular and longitudinal fibers, as would be seen in a rhabdocoel like a typhloplanoid or dalyellioid species, are represented, but many variations on this theme apply to the free-living flatworms in general. The space between the body wall and gut could be filled with parenchymal cells, the cell bodies of epidermal glands, or internal organs such as gonads. The gut could also have its own musculature as indicated in the lower part of the Figure. (Based on a scheme by Rieger and Ladurner 2001.) (B) Schematic representation of the body wall of adult neodermatan flatworms (Neodermata) as seen in a longitudinal section of the body and subdivided to represent typi- cal surface specializations associated with four major groups of the taxon. Diagonal muscle fibers lie innermost, as opposed to between the other two muscle layers as in Fig. 1A. called a neodermis (for “new skin”; Ehlers 1985), in the cells, also arise from such neoblasts in flatworms; no differ- course of infecting a new host. entiated somatic cells in the body are capable of dividing The mode of replacement of the epidermis, whether as (Peter et al. 2001). part of growth or general maintenance of the epidermis or Without an autapomorphy such as the neoblast, there is the development of the neodermis, appears to be unique to some justification for questioning the monophyletic nature the Platyhelminthes. Rather than arising from dividing cells of the phylum Platyhelminthes (Smith et al. 1986) and, in within the epidermis, as appears to be the case for other fact, recent proposals based on molecular data are to place metazoans, new epidermal cells arise from stem cells, the two orders of platyhelminths, the Acoela and Nemerto- neoblasts, that reside below the body wall and then migrate dermatida, into separate phyla outside the Platyhelminthes into the epidermis as they differentiate. This developmental (Ruiz-Trillo et al. 1999; Jondelius et al. 2002; Ruiz-Trillo et mode applies even in embryogenesis of the turbellarians al. 2002). Other morphological data support the monophy- (i.e., embryonic and definitive epidermises grow by immi- letic nature of at least three clades within the Platyhelmin- gration of stem cells from underlying layers) and is the way thes: the Acoelomorpha, Catenulida, and Rhabditophora. in which each new generation of neodermis arises as larval The Acoelomorpha, comprising the Acoela and Nemertoder- stages develop in sequence in the more complex parasitic matida, share features of epidermal ultrastructure (the form life cycles of neodermatans (Tyler and Tyler 1997). The of the cilia and their rootlets), as well as of certain glands neoblast stem cell system, and particularly its role in re- (Tyler and Rieger 1977; Smith and Tyler 1985; Smith et al. newal of the epidermis, may in fact be an autapomorphic 1986; Ehlers 1992a). The acoels, which have often figured trait for the Platyhelminthes (Rieger and Ladurner 2001). in phylogenetic hypotheses of the origin of the Bilateria, are Muscles of the body wall, as well as all other differentiated mostly small marine worms with a digestive system consist- © 2004 NRC Canada 196 Can. J. Zool. Vol. 82, 2004 ing of a syncytium (and so lacking a lumen, hence the name Two belt-form junctions join each cell to its neighbors: an Acoela). The Catenulida, a small group containing a strange apical-most zonula adherens and, just basal to this, a septate primitive marine family but mostly freshwater species, share junction (Fig. 2D). Spot-form junctions, namely hemiadher- a special orientation and position of the male reproductive ens junctions, link the cells to the underlying basal lamina and excretory organs (Smith et al. 1986). The rest of the (Figs. 2A and 2C). The zonula adherens links prominently platyhelminths, including the parasitic classes and such well- with the actin filaments of the terminal web. Actin filaments known free-living groups as the planarians (Tricladida) and also compose stress-fiber bundles that anchor basally to the polyclads, form the monophyletic group Rhapditophora and hemiadherens junctions. share features (at least primitively) including adhesive or- All general epidermal cells are multiciliated and their cilia gans and rhabdite glands. anchor into the cytoplasm by two rootlets, a tubular rostral In all three clades, neoblasts residing below the body wall rootlet extending from the rostral side of the ciliary basal give rise to other cells, including those involved in growth body and a solid-cored vertical rootlet extending from its and replacement of the epidermis. The body wall and its re- basal end and penetrating the terminal web (Fig. 2A). lation to these stem cells may provide the best characters for Microvilli between the cilia bear a glycocalyx that forms a reuniting these three clades into the single phylum Platyhel- diffuse mucous coat over the epithelial surface.
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