Platyhelminthes and Acoelomorpha---phyla of controversy

by Seth Tyler ©2004
University of Maine

drawing of representative Acoel, Catenulid, and Rhabditophoran
Representative worms from the three major monophyletic groups of flatworms: the Acoelomorpha (represented by an acoel turbellarian), the Catenulida (represented by a retronectid turbellarian), and the Rhabditophora (represented by a digenetic trematode)

The relatively small worms that are commonly called flatworms are classified in the phyla Platyhelminthes, whose Greek roots mean, in fact, "flat worm," and the Acoelomorpha, recently removed from the Platyhelminthes into its own phylum. In general, the flatworms

They thus stand distinct from the major phylum of worms, the Annelida, whose members have a complete gut (with anus as well as mouth), segmented bodies with fluid-filled coelomic compartments, a cuticle-covered body wall, muscles that arise from epithelial mesodermal tissue, and monoflagellated sperm (as do most other animals). But other phyla of small worms share some of the characters that otherwise set flatworms apart. Hermaphroditism, with reproductive organs as complicated as those of the flatworms, appear in the Gnathostomulida and Gastrotricha, for instance. Lack of a cuticle covering the body wall is also a feature of the Gnathostomulida (though the jaws of gnathostomulids are true cuticular elements which are completely lacking in flatworms), and so, too, is a sack-like gut a feature of the gnathostomulids (but it appears to be derived from a complete gut by virtue of evidence for a vestigial anus in gnathostomulids). Other worm phyla have cuticle (Gastrotricha, Nematoda, Nematomorpha, Kinorhyncha, Priapulida, etc.), multiciliated epidermal cells (all worm phyla but the Gnathostomulida), solid (acoelomate) bodies (Gastrotricha and miscellaneous representatives of Nematoda, Annelida, etc.), and fiber-form muscle cells. And though obviously a convergent similarity, the character of biflagellate spermatozoa is seen in some groups of fishes.

Nevertheless, the characteristics we can list for flatworms are not absolute distinctions--none apply to all flatworms together to the exclusion of other animals. Because no overarching characteristics (synapomorphies) for flatworms as a whole can be identified unequivocally, there is ground for considering the Platyhelminthes not to be a valid monophyletic phylum (Smith et al., 1986; Baguñà and Riutort, 2004). At the moment, the largest monophyletic groups that can be identified among flatworms are three, the Acoelomorpha, the Catenulida, and the Rhabditophora, and while any two of these may be related as sister groups, the characters we could use to tie those two would exclude the third from falling into a logical phylogenetic relation with them. For example, the Catenulida and Rhabditophora appear to share homologies in the structure of the epidermal ciliary rootlets, in the mechanism by which they replace their epidermal cells, and in having protonephridia, but these homologies do not extend to the Acoelomorpha. The Acoela, on the other hand, appears to share with the Rhabditophora the homology of biflagellate spermatozoa, but since catenulids don't have such sperm (and since the Nemertodermatida, the sister group to the Acoela in the Acoelomorpha, also lack such sperm), this homology would negate those homologies listed between Catenulida and Rhabditophora. The Acoelomorpha shares no apomorphies with both the Catenulida and Rhabditophora except possibly the presence of special stem cells called neoblasts (Rieger and Ladurner, 2001). Because the most recently analyzed molecular characters indicate a rather distant relationship between the Acoelomorpha and the other flatworms (see below), it has been removed as a separate phylum, leaving Catenulida and Rhabditophora together by default in the phylum Platyhelminthes. (See current classification system for the flatworms).

drawing of representative Acoela, Catenulida, Macrostomida and Proseriata
Turbellarian platyhelminths; representatives of 4 of the 11 orders of turbellarians

The more traditional classification of flatworms places them all in the phylum Platyhelminthes in four classes: Turbellaria, Monogenea, Trematoda, and Cestoda. Turbellarians are the largely free-living flatworms, those that don't parasitize other animals, while the other classes encompass the obligate parasites. Eleven orders of turbellarians are recognized in the commonly used classification that Hyman championed (Tyler, 1999): Nemertodermatida, Acoela, Catenulida, Haplopharyngida, Macrostomida, Polycladida, Lecithoepitheliata, Prolecithophora, Rhabdocoela, Proseriata, and Tricladida). Monogeneans are largely ectoparasites on vertebrates like fishes; trematodes are the flukes, most of which live inside the organs of vertebrates as adults; and cestodes are the tapeworms, living in the intestines of vertebrates as adults. Turbellaria is, in particular, considered an invalid class because it is not monophyletic. (It is either paraphyletic in that the parasitic classes arose from an ancestor that would be classified within the Turbellaria [Ehlers, 1985] or it is polyphyletic if the acoels and the rhabditophorans arose from two distinct ancestors [Baguñà and Riutort, 2004]). The term "turbellarian" is still a useful moniker referring to all those worms formerly classified in the Turbellaria, but the term "Turbellaria" (specifically, the capitalized taxon name) would have to be written in quotation marks to indicate its paraphyletic status. Not all turbellarians are free-living, and so "free-living plathelminths," another name often applied to them by cladists wishing to avoid "Turbellaria," has some disadvantages; there are some highly specialized parasites among virtually all subgroups of the turbellarians (Jennings, 1971, 1997).

drawing of Kalyptorhynchia, Polycladida, Tricladida
Turbellarian platyhelminths; representatives of another three orders of turbellarians

The quintessential parasitic flatworms are the monogeneans, trematodes, and cestodes, and these constitute monophyletic groups, but by a cladistic classification, these monophyletic groups would not have the rank of class. Instead, if any monophyletic groups are to be considered classes, they would have to be the three major groups constituting the former "Turbellaria," namely the Catenulida and Rhabditophora (and Acoelomorpha, if that is to retained in the Platyhelminthes). The major parasitic groups lie within the Rhabditophora, specifically within the monophyletic taxon Neodermata in that class. They are clearly closely related, descended from a common ancestor among the turbellarians.

drawing of Monogenea, Cestoda, Digenea
Representatives of the three major groups of Neodermata (a tapeworm, a digenetic trematode, and a monogenean)

Exactly where the Neodermata came from among turbellarian platyhelminths is not at all clear; a number of potential ancestral groups have been proposed (Ehlers, 1985; Brooks, 1989; Littlewood et al., 1999; Lockyer et al., 2003; Baguñà and Riutort, 2004). The major advancement that allowed them to adopt a parasitic existence seems to be the neodermis which arises as the parasites attack a new host and metamorphose from the free-living larva. That larva has an epidermis much like that of turbellarians, composed of ciliated cells. When it locates a host, the larva sheds this ciliated epidermis and a new epidermis, the neodermis, emerges from cells situated below the muscle layer of the body wall. These cells fuse to create a syncytial covering over the entire body. The neodermis, thus, is an uninterrupted layer of syncytium whose nuclei lie in cytons below the body-wall musculature; on its apical surface facing the environment are specialized microvilli-like projections whose shape is specialized in each of the neodermate groups. The neodermis must offer advantages in a parasitic existence, allowing the parasite to absorb nutrients from the host (cestodes have, in fact, dispensed with the mouth and gut and gain all their nutrients from the host by absorption through the neodermis) and probably serving a dynamic role in defeating host immune reactions. Platyhelminths seem to be preadapted to developing such an epidermis in that even the turbellarians go through successive generations of epidermis in their embryonic development, and as adults they regenerate their epidermis by repacing cells that are lost with cells that migrate into it from the parenchyma below the muscles (Tyler and Tyler 1997).





[The position of the Acoela and the validity of the phylum Acoelomorpha remain unsettled. See Egger et al. 2009.]



References

Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489-493

Baguñà J, Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Riutort M (2001) The first bilaterian organisms: simple or complex? New molecular evidence. Int J Dev Biol 45: S133-S134.

Baguñà J, Riutort M (2004) Molecular phylogeny of the Platyhelminthes. Can J Zool 82:168-193.

Berney C, Pawlowski J, Zaninetti L (2000) Elongation factor 1-alpha sequences do not support an early divergence of the Acoela. Mol Biol Evol 17:1032-1039.

Blair JE, Ikeo K, Gojobori T, Hedges SB (2002) The evolutionary position of nematodes. BMC Evolutionary Biol http://www.biomedcentral.com/1471-2148/2/7

Brooks DR (1989) The phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela) and general evolutionary principles. J Parasitology 75: 606-616.

Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203-266

Haszprunar G (1996) Plathelminthes and Plathelminthomorpha -- paraphyletic taxa. J Zool Syst Evol Res 34:41-48

Hendelberg J, Hedlund K-O (1974) On the morphology of the epidermal ciliary rootlet system of the acoelous turbellarian Childia groenlandica. Zoon 2:13-24.

Hooge MD, Haye P, Tyler S, Litvaitis MK, Kornfield I (2002) Molecular systematics of the Acoela (Platyhelminthes) and its concordance with morphology. Molecular Phylogeny and Evolution 24:333-342

Jennings JB (1971) Parasitism and commensalism in the Turbellaria. In: Advances in Parasitology, vol 9 (ed. Ben Dawes):1-32. Academic Press, New York.

Jennings JB (1997) Nutritional and respiratory pathways to parasitism exemplified in the turbellaria. Int. J Parasitology 27: 679-691.

Joffe BI, Kornakova EE (2001) Flatworm phylogeneticist: between molecular hammer and morphological anvil. In: Littlewood T, Bray R, eds. Interrelationships of the Platyhelminthes. Taylor & Francis, London. pp 279-291

Jondelius U, Ruiz-Trillo I, Baguñà J, Riutort M (2002) The Nemertodermatida are basal bilaterians not members of Platyhelminthes. Zool Scr 31:201-215

Ehlers U (1985) Das Phylogenetische System der Plathelminthes. Gustav Fischer, Stuttgart, New York. 317 pp

Ehlers U (1992) On the fine structure of Paratomella rubra Rieger & Ott (Acoela) and the position of the taxon Paratomella Dörjes in a phylogenetic system of the Acoelomorpha (Plathelminthes). Microfauna Mar 7:265-293.

Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linnean Soc 66: 75-114

Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155-171.

Lundin K (1997) Comparative ultrastructure of the epidermal ciliary rootlets and associated structures in species of the Nemertodermatida and Acoela (Plathelminthes). Zoomorphology 117:81-92

Pennisi E (2003) Modernizing the Tree of Life. Science 300:1692-1697.

Reuter M, Raikova OI, Jondelius U, Gustafsson MKS, Maule AG, Halton DW (2001) Organisation of the nervous system in the Acoela: an immunocytochemical study. Tissue Cell 33:119-128

Rieger RM, Tyler S, Smith JPS III, Rieger GE (1991) Platyhelminthes: Turbellaria. In: FW Harrison & BJ Bogitsh (eds) Microscopic Anatomy of Invertebrates. Vol. 3: Platyhelminthes and Nemertinea. Wiley-Liss, New York: 7-140

Rieger RM (1994) The biphasic life cycle -- a central theme of metazoan evolution. Am Zool 34:484-491

Rieger RM (1986) Ueber dem Ursprung der Bilateria: die Bedeutung der Ultrastrukturforschung fuer ein neues Verstehen der Metazoenevolution. Verh Dtsch Zool Ges 79:31-50

Ruiz-Trillo I, Riutort M, Littlewood DTJ, Hernieu EA, Baguñà (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283:1919-1923

Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Baguñà J, Riutort M (2002) A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertoderematida are basal bilaterians. PNAS 99:11246-11251

Smith JPS (1981) Fine-structural anatomy of the parenchyma in the Acoela and Nemertodermatida (Turbellaria). Ph.D. Dissertation, Univ North Carolina, Chapel Hill.

Smith JPS, Tyler S (1985) The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot? In: Conway Morris C, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Oxford University Press, Oxford, pp 123-142

Smith JPS, Tyler S, Rieger RM (1986) Is the Turbellaria polyphyletic? Hydrobiologia 132:13-21

Sterrer W, Rieger RM (1974) Retronectidae--a new cosmopolitan marine family of Catenulida (Turbellaria). In: Riser NW, Morse MP (eds) Biology of the Turbellaria. McGraw-Hill, New York: 63-92.

Telford MJ, Lockyer AE, Cartwright-Finch C, Littlewood DTJ (2003) Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc R Soc Lond B 270:1077-1083

Tyler S (1979) Distinctive features of cilia in metazoans and their significance for systematics. Tissue Cell 11:385-400.

Tyler S (1999) Systematics of the flatworms--Libbie Hyman's influence on current views of the Platyhelminthes. Am Mus Novitates 3277: 52-66

Tyler S (2001) The early worm--origins and relationships of the lower flatworms. In: Interrelationships of the Platyhelminthes. Littlewood DTJ, Bray R (eds). Taylor & Francis, London. pp 3-12.

Tyler S, Rieger RM (1977) Ultrastructural evidence for the systematic position of the Nemertodermatida (Turbellaria). Acta Zool Fennica 54:193-207

Tyler S, Tyler MS (1997) Origin of the epidermis in parasitic platyhelminths. Int J Parasitol 27: 715-738

Tyler S, Hooge M (2004) Comparative morphology of the body wall in flatworms (Platyhelminthes). Can J Zool 82:194-210.


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