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Platyhelminthes) Proc. Helminthol. Soc. Wash. 52(1), 1985, pp. 1-20 The Phylogeny of the Cercomeria Brooks, 1982 (Platyhelminthes) DANIEL R. BROOKS, RICHARD T. O'GRADY, AND DAVID R. GLEN Department of Zoology, University of British Columbia, 2075 Westbrook Mall, Vancouver, B.C. V6T 2A9, Canada ABSTRACT: A new classification of the parasitic platyhelminths is presented. It is derived by phylogenetic analysis of 39 morphological characters drawn from 19 putative homologous series. The construction and interpretation of phylogenetic trees using Hennigian phylogenetic systematics is discussed briefly to provide a reference point for the conclusions drawn. Parasitic platyhelminths having, at some time in ontogeny, a posterior adhesive organ formed by an expansion of the parenchyma into, minimally, an external pad, form the subphylum Cercomeria. Three superclasses are recognized within the Cercomeria: the Temnocephalidea, which is the most plesiomorphic of the three; the Udonellidea; and the Cercomeridea. Within the Cercomeridea, two classes are recognized: the Trematoda and the Cercomeromorphae. The Trematoda contains two subclasses, the Aspidocotylea and the Digenea, and the Cercomeromorphae contains the Monogenea, Gyrocotylidea, Amphilinidea, and Eucestoda. The Monogenea is the sister-group of the latter three, which together form the Cestodaria. The Gyrocotylidea is the sister group of the Amphilinidea and Eucestoda, which together form the Cestoidea. Several of the character complexes examined are discussed in detail, and all are listed. The number of hooks on the larval cercomer is concluded to be of little help in analyzing phylogenetic relationships among the cercomeromorphs. Other characters are more informative and provide additional support for the phylogeny proposed herein. These include the relative positions of the genital openings, and the structure of the anterior and posterior parts of the nervous system. New homologies are proposed for posterior adhesive organs and anterior body invaginations. The complex life cycles of digeneans and eucestodes are concluded to differ from each other in manner of origin. Eucestodes exhibit terminal addition of ontogenetic stages and nonterminal addition of an invertebrate host. Digeneans exhibit nonterminal addition of ontogenetic stages and terminal addition of a vertebrate host. Com- parison of the classification presented with eight previous classifications shows that it provides the best fit to the data considered. In the past 75 years there have been at least posed that parasitic platyhelminths possessing a eight proposals for the phylogenetic relationships posterior adhesive organ be included in a sub- and classification of the parasitic platyhelminths. phylum, the Cercomeria. This study extends and Two of the earliest, by Sinitsin (1911) and Fuhr- supports that hypothesis. mann (1928, 1931), postulated a dichotomy be- tween those with a gut and those without a gut. Materials and Methods The remaining six studies (Spengel, 1905; Jani- To provide a reference point for some of the con- cki, 1920; Bychowsky, 1937, 1957; Llewellyn, clusions we will draw, we present a precis of the theory 1965; Price, 1967;Malmberg, 1974) viewed those and methodology of Hennigian phylogenetic system- with a gut as either paraphyletic or polyphyletic. atics. See Wiley (198la) and Brooks et al. (1984) for a more complete discussion. This precis is followed by No general agreement has emerged. The present a list of the characters we analyzed, as well as a brief study is an application of Hennigian phyloge- discussion of diagnoses and keys. netic systematics (Hennig, 1950, 1966) to the Phylogenetic systematics problem. Organisms from different species may resemble each Previous attempts at phylogenetic analysis of other by possessing similar traits that either have been certain parasitic platyhelminths (Brooks, 1977, inherited from a common ancestor or have evolved 1978a, b, 1981a; Brooks and Overstreet, 1978; independently. The first types of traits are homologies, Brooks et al., 198 la, b; Brooks and Caira, 1982) the second types are analogies. In a system produced by evolution, only homologies indicate phylogenetic have been hampered by the lack of well-corrob- (i.e., genealogical) relationships; thus, only homologies orated outgroups (see the next section). This has can be used for a phylogenetic classification. Given that made character analysis difficult. Before attempt- homologues covary in greater numbers than do ana- ing more analyses of particular groups, we con- logues, such a classification will be the most efficient sidered it necessary to construct an hypothesis information storage and retrieval system for system- atics (see Farris, 1979; Brooks, 1981b). of the higher level relationships among the platy- Phylogenetic systematics avoids two types of ad hoc helminths. Brooks (1982) provided a brief dis- assumptions that can be introduced into classificatory cussion of the results presented here, and pro- studies. The first is the use of a unique trait to highlight 1 Copyright © 2011, The Helminthological Society of Washington PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY a particular taxon, with the concomitant grouping of Phylogenetic classifications are based on the discov- the remaining taxa. Unique traits do set a taxon off by ery of appropriate levels of generality for homologous itself, but it does not follow that the remaining taxa traits, and the recognition of groupings supported by not so highlighted form an evolutionary group. The synapomorphic traits. A number of protocols have been second type of ad hoc assumption concerns explana- advanced for determining the plesiomorphy and apo- tions of ambiguities in the data. Ambiguities are caused morphy of traits in a study group (see, e.g., Stevens, by homoplasy, or parallel and convergent evolution, 1980). To date all have been found either to be capable which is not recognized as such beforehand. This is of giving incorrect estimates (such as the principle of caused by the independent acquisition or loss of a trait "common equals primitive" of Estabrook, 1971,1978, by two or more species. Homoplasious characters allow and Crisci and Stuessy, 1980), or to be special cases of more than one classification to be inferred from the the more general method of "outgroup comparisons." same data set. They will be inconsistent with the phy- Outgroup comparisons are based on the concept that logenetic classification that explains their true origins, a trait found in at least one member of the study group and consistent with at least one classification based on and in a taxon outside the group (the outgroup—a close particular parallel or convergent traits. For example, relative of the group being analyzed) is plesiomorphic. in a group of organisms in which a trait is primitively Such a trait is considered to have evolved prior to the absent, then evolves, and then is lost by some mem- existence of the ancestral species from which the study bers, those lacking the trait could all be classified to- group evolved. By contrast apomorphic traits are those gether, or they could be classified separately to recog- found only in some members of the study group. Be- nize the primitive and derived conditions. cause outgroups can themselves evolve, it is sometimes Phylogenetic systematics recognizes that both of the necessary to use more than one outgroup to confirm above problems require additional data for their res- the plesiomorphy of a trait (Wiley, 198 la). olution. It eliminates the first type of ad hoc reasoning by grouping taxa only by shared derived characters. Homologous series of platy helminth Unique derived characters may be reported in a taxon's characters examined diagnosis, but they are not used to make groupings. Nineteen kinds of larval and adult platyhelminth The second type of ad hoc reasoning is minimized by traits are given below. Each is considered to be a po- considering the largest subset of the data that covaries tential series of homologues produced through evolu- in a single pattern to consist of homologous traits, and tionary transformation. Each component of a series is the exceptions to that pattern to indicate true homo- a character. It is these characters (e.g., bifurcate gut), plasy. Phylogenetic systematics thus neither denies the rather than the series (e.g., intestine), that individual existence of homoplasy, nor assumes its rarity. Its only taxa display. Homologous series may consist of two assumption is that these false indicators of phylogeny characters (e.g., the presence or absence of locomotor do not themselves covary in a pattern better supported cilia) or more (e.g., the various types of posterior ad- than that of the homologues. hesive organs). The derived state of a two-state series Three levels of homologous traits may be discerned. will be a shared derived character for a single mono- Some may be found in all members of a group being phyletic group. A multistate character is produced when classified. These help establish that group's identity, the derived character of a two-state series undergoes but give no clues to the relationships of its members. further evolution. This may produce either further Others may be present in all individuals of one member structural modification or loss (vs. primitive absence) taxon, but absent in the rest. These establish the iden- of the character. The result is an internesting of mono- tity of single taxa, but provide no clues to relationships phyletic groups (decreasing inclusiveness
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