The phylogeny of the cercomeria Brooks, 1982 (Platyhelminthes, DR Brooks, RT O'Grady, DR Glen

Tags: Helminthological Society, Washington, J. Parasitol, New York, pp, characters, phylogenetic tree, vertebrate host, convergent evolution, study group, genital pores, Academic Press, New York Botanical Garden, uterine pore, D. R. Brooks, J. Zool, hooks, classification, classifications, Phylogenetic Systematics, genital pore, Superclass Udonellidea Ivanov, anterior and posterior, S. S. Desser, invertebrate host, Subclass Cestodaria Monticelli, Subclass Aspidocotylea Monticelli, Superclass Temnocephalidea Benham, cestodes, T. Krumbach, Walter de Gruyter, addition, evolutionary sequences, anterior commissure, digestive system, nervous system, posterior commissure, central nervous system, intermediate host, developmental stages, larval stages, Copyright, morphological characters, evolutionary differences, Author Fuhrmann, plesiomorphic, Platyhelminthes
Content: 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, ANDDAVID 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. Comparison 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 eight proposals for the phylogenetic relationships and classification of the parasitic platyhelminths. Two of the earliest, by Sinitsin (1911) and Fuhrmann (1928, 1931), postulated a dichotomy between those with a gut and those without a gut. The remaining six studies (Spengel, 1905; Janicki, 1920; Bychowsky, 1937, 1957; Llewellyn, 1965; Price, 1967;Malmberg, 1974) viewed those with a gut as either paraphyletic or polyphyletic. No general agreement has emerged. The present study is an application of Hennigian phylogenetic systematics (Hennig, 1950, 1966) to the problem. Previous attempts at phylogenetic analysis of certain parasitic platyhelminths (Brooks, 1977, 1978a, b, 1981a; Brooks and Overstreet, 1978; Brooks et al., 198 la, b; Brooks and Caira, 1982) have been hampered by the lack of well-corroborated outgroups (see the next section). This has made character analysis difficult. Before attempting more analyses of particular groups, we considered it necessary to construct an hypothesis of the higher level relationships among the platyhelminths. Brooks (1982) provided a brief discussion of the results presented here, and pro-
posed that parasitic platyhelminths possessing a posterior adhesive organ be included in a sub- phylum, the Cercomeria. This study extends and supports that hypothesis. Materials and Methods To provide a reference point for some of the conclusions we will draw, we present a precis of the theory and methodology of Hennigian phylogenetic systematics. See Wiley (198la) and Brooks et al. (1984) for a more complete discussion. This precis is followed by a list of the characters we analyzed, as well as a brief discussion of diagnoses and keys. Phylogenetic systematics Organisms from different species may resemble each other by possessing similar traits that either have been inherited from a common ancestor or have evolved independently. The first types of traits are homologies, the second types are analogies. In a system produced by evolution, only homologies indicate phylogenetic (i.e., genealogical) relationships; thus, only homologies can be used for a phylogeneticclassification. Given that homologues covary in greater numbers than do analogues, such a classification will be the most efficient information storage and retrieval system for systematics (see Farris, 1979; Brooks, 1981b). Phylogenetic systematics avoids two types of ad hoc assumptions that can be introduced into classificatory studies. The first is the use of a unique trait to highlight
1
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a particular taxon, with the concomitant grouping of the remaining taxa. Unique traits do set a taxon off by itself, but it does not follow that the remaining taxa not so highlighted form an evolutionary group. The second type of ad hoc assumption concerns explanations of ambiguities in the data. Ambiguities are caused by homoplasy, or parallel and convergent evolution, which is not recognized as such beforehand. This is caused by the independent acquisition or loss of a trait by two or more species. Homoplasious characters allow more than one classification to be inferred from the same data set. They will be inconsistent with the phylogenetic classification that explains their true origins, and consistent with at least one classification based on particular parallel or convergent traits. For example, in a group of organisms in which a trait is primitively absent, then evolves, and then is lost by some members, those lacking the trait could all be classified together, or they could be classified separately to recognize the primitive and derived conditions. Phylogenetic systematics recognizes that both of the above problems require additional data for their resolution. It eliminates the first type of ad hoc reasoning by grouping taxa only by shared derived characters. Unique derived characters may be reported in a taxon's diagnosis, but they are not used to make groupings. The second type of ad hoc reasoning is minimized by considering the largest subset of the data that covaries in a single pattern to consist of homologous traits, and the exceptions to that pattern to indicate true homoplasy. Phylogenetic systematics thus neither denies the existence of homoplasy, nor assumes its rarity. Its only assumption is that these false indicators of phylogeny do not themselves covary in a pattern better supported than that of the homologues. Three levels of homologous traits may be discerned. Some may be found in all members of a group being classified. These help establish that group's identity, but give no clues to the relationships of its members. Others may be present in all individuals of one member taxon, but absent in the rest. These establish the identity of single taxa, but provide no clues to relationships with other Group Members. Finally, there may be homologues shared by two or more of the taxa in the study group. These indicate particular relationships within the group. Traits that are general to the group being studied are plesiomorphies. Those found only within part of the study group and not in any taxa outside the group are apomorphies. Shared plesiomorphies are symplesiomorphies. Unique apomorphies are autapomorphies. Shared apomorphies are synapomor- phies. Two aspects of phylogenetic systematics make this nomenclature necessary. First, Hennig rejected "idealized morphology" and its stress on the search for archetypal forms, and postulated that any species is a composite of ancestral and derived traits. Second, traits produced as novelties at one time can become generalized traits of a descendant group. Plesiomorphy and apomorphy therefore refer to relative primitiveness and derivation, depending on the level of generality of the investigation. For example, hair is a synapomorphy (shared derived trait) for mammals when discussing tetrapod evolution, but a symplesiomorphy (shared ancestral trait) when discussing the evolution of rodents.
Phylogenetic classifications are based on the discovery of appropriate levels of generality for homologous traits, and the recognition of groupings supported by synapomorphic traits. A number of protocols have been advanced for determining the plesiomorphy and apomorphy of traits in a study group (see, e.g., Stevens, 1980). To date all have been found either to be capable of giving incorrect estimates (such as the principle of "common equals primitive" of Estabrook, 1971,1978, and Crisci and Stuessy, 1980), or to be special cases of the more general method of "outgroup comparisons." Outgroup comparisons are based on the concept that a trait found in at least one member of the study group and in a taxon outside the group (the outgroup--a close relative of the group being analyzed) is plesiomorphic. Such a trait is considered to have evolved prior to the existence of the ancestral species from which the study group evolved. By contrast apomorphic traits are those found only in some members of the study group. Because outgroups can themselves evolve, it is sometimes necessary to use more than one outgroup to confirm the plesiomorphy of a trait (Wiley, 198 la). Homologous series of platy helminth characters examined Nineteen kinds of larval and adult platyhelminth traits are given below. Each is considered to be a potential series of homologues produced through evolutionary transformation. Each component of a series is a character. It is these characters (e.g., bifurcate gut), rather than the series (e.g., intestine), that individual taxa display. Homologous series may consist of two characters (e.g., the presence or absence of locomotor cilia) or more (e.g., the various types of posterior adhesive organs). The derived state of a two-state series will be a shared derived character for a single monophyletic group. A multistate character is produced when the derived character of a two-state series undergoes further evolution. This may produce either further structural modification or loss (vs. primitive absence) of the character. The result is an internesting of monophyletic groups (decreasing inclusiveness of taxa), each of which inherited a particular character of the series. The discovery of this internesting is made possible by determining the relative primitiveness and derivation of the characters. Outgroup comparisons help to establish the direction, or polarization, of this transformation. a. LOCOMOTOR CILIA: Among platyhelminths adult dalyelloid rhabdocoels exhibit restricted locomotor cilia, whereas adults of the Temnocephalidea, Udonellidea, and the trematode and cercomeromorphan groups (sensu nobis) lack locomotor cilia altogether (see Williams, 1981). The secondary loss of cilia in adult cercomerians is further corroborated by the presence of ciliated larvae in some members of all groups. b. VAGINA: In dalyelloids and temnocephalideans a single duct extends from the ovary. In some taxa this duct joins the uterus, and in others it opens directly into the genital atrium. Udonellideans, trematodes (sensu nobis) and cercomeromorphs (sensu nobis) possess two ducts extending from the ovary. One of these connects with the uterus, contains the ootype region, and receives the vitelline ducts. The other duct may open to the exterior by means of a separate pore or a
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common atrium. Following traditional terminology, we call the first duct the oviduct (Hyman [1951] called it the ovovitelline duct), and the second the vagina. We do not believe that this vaginal duct has a counterpart among other turbellarians. Udonellideans, gyrocotylideans, amphilinideans, and eucestodes possess well-developed vaginae. Digeneans and aspidocotyleans have a small duct, called the Laurer's canal, extending from the oviduct region. This usually opens to the dorsal surface, but can end blindly in either taxon (almost always in aspidocotyleans), or connect with the excretory system (in some aspidocotyleans). Monogeneans have paired lateral vaginal openings, with apparent secondary loss of vaginae in many groups. c. OVARY ANDTESTES NUMBER:Dalyelloids have single ovaries and paired testes. Among various groups of parasitic platyhelminths, testes number has either decreased to one, or increased to many. The dalyelloid condition is nevertheless found in some temnoceph- alideans, digeneans, aspidocotyleans, and monogeneans. Because of the widespread occurrence of changes in testes number, we have not used any of the derived states in our analysis. d. EXCRETORY SYSTEM: Paired lateral excretory ducts joining posteriorly into a vesicle comprise an additional trait linking dalyelloids with the rest of the parasitic platyhelminths. e. PHARYNX: The doliiform pharynx (barrel-shaped, see Hyman, 1951) found in dalyelloid rhabdocoels occurs in temnocephalideans, udonellideans, digeneans, aspidocotyleans, and monogeneans. It has generally been considered that there is no pharynx in gyrocotylideans, amphilinideans and eucestodes (but see Discussion). f. COPULATORY STYLET: Some form of sclerotized copulatory apparatus is part of the male genitalia of dalyelloids, temnocephalideans, udonellideans, and monogeneans. Digeneans, aspidocotyleans, gyrocotylideans, amphilinideans, and eucestodes lack such structures. g. INTESTINE: Dalyelloids have a saccate gut, as do the majority of turbellarians. This trait is found in temnocephalideans, udonellideans, and most aspidocotyleans. Digeneans and monogeneans, for the most part, possess bifurcate guts. Gyrocotylideans, amphilinideans, and eucestodes lack a gut. h. MEHLIS' GLAND: This gland is lacking in dalyel- loids, at least as a centralized glandular structure. Although it is not unambiguouslyclear that temnocephalideans possess this gland (see Williams, 1981), all other groups in this study have been shown to have it. i. POSTERIOR ADHESIVE ORGAN: Posterior attachment structures in the platyhelminths consist of adhesive glandular secretions, suckers, and hooks (see Hyman, 1951). The first primarily involve tegumental modifications, and the other two involve extensive parenchymal modifications as well. Adhesion can thus be achieved by chemical action, vacuum principle, and mechanical embedding, respectively. There appear to be four basic types of morphological modifications to the posterior holdfast organ: (1) glandule-epidermal secretions, (2) expansion of the parenchyma into an external "pad" of some sort, (3) development of suckers by muscularization of the pad, and (4) the presence of hooks. Different combinations of these modifica-
Table 1. The four basic modifications to the posterior adhesive organ in the platyhelminth taxa studied. Adhesive secretions are produced by glandule-epidermal modifications, whereas the remaining three traits involve parenchymal modifications as well. The expansion of the parenchyma into an external "pad" at the posterior end of the body is considered to mark the first appearance of a cercomer. This organ is relatively unmodified in the Temnocephalidea and Udonellidea, and augmented with muscularization and/or hooks in the more derived taxa.
Dalyelloidea Temnocephalidea Udonellidea Aspidocotylea Digenea Monogenea Gyrocotylidea Amphilinidea Eucestoda
PaAdhe- renchysive mal secre- expan- Mustions sion cles
Hooks
tions exist in the taxa studied (see Table 1). Dalyelloids (e.g., Dalyellia; see Hyman, 1951) have only glandular secretions (see also the discussion for behavioral observations). Temnocephalideans and udonellideans have a parenchymal expansion as well (Williams, 1981). In digeneans this expansion has become muscularized to form a sucker that is midventral in many species, but posterior in a number of apparently primitive groups. Aspidocotyleans possess a posterior ventral sucker early in ontogeny that becomes a rugose or loculate disk in the adults. The adhesive organ reaches its maximum complexity in monogeneans, which possess hooks in addition to the three earlier modifications. The early larval stages of gyrocotylideans, amphilinideans, and eucestodes possess a posterior expansion bearing hooks, but apparently lacking adhesive secretions. The hooks may persist in a disar- rayed configuration near the dorsal pore of the rosette funnel in gyrocotylidean adults (e.g., Gyrocotyle urna; see Lynch, 1945) and at the rounded posterior end of the body in amphilinidean adults (e.g., Austramphilina elongata; see Rohde and Georgi, 1983). j. TENTACLES: Temnocephalideans possess tentacles on their anterior ends, although in some cases these may be very small and possibly secondarily reduced (Williams, 1981). Some digenean (e.g., bucephalids) and eucestode (trypanorhynchs) groups possess "tentacles" as well, but these are neither common to all digeneans and eucestodes, nor of the same structure as those in temnocephalideans. k. GENITAL PORES LOCATION: Turbellarians possess genital pores at the posterior end of the body. With the exception of amphilinideans the rest of the taxa in this study generally have all genital pores in or near the anterior half of the body, or proglottid (in eucestodes).
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Amphilinideans have the male pore and the vagina in the posterior half, and the uterine pore in the anterior half (see Fig. 3). 1. GENITAL PORES ASSOCIATION: In dalyelloids and many other turbellarians the genital openings occur together, often in a common genital atrium. In the digeneans and monogeneans the vagina is separate from the male and uterine openings. The latter two may open to a common genital atrium and exit through a common genital pore. In the aspidocotyleans the vaginal opening is lacking altogether, but the relative positions of the male opening and uterine pore are as in digeneans. Gyrocotylideans have all three genital pores separated but in close proximity in the anterior half of the body. Amphilinideans have the uterine pore in the anterior half of the body, and the vagina and male pore separate in the posterior end of the body. Eucestodes possess closely associated male and vaginal openings (see Fig. 3). m. ORAL SUCKER: Most digeneans, aspidocotyleans, and monogeneans have oral suckers. Gyrocotylideans, amphilinideans, and eucestodes possess, at some period in ontogeny, invaginations at the anterior end that we interpret as vestigial mouths and associated structures (see Discussion). n. LIFE CYCLE PATTERNS: All of the platyhelminths considered here are associated with a host of some sort. Temnocephalideans, udonellideans, and aspidocotyleans are associated primarily with invertebrates; although some aspidocotyleans occur in vertebrates, these hosts are not necessary for completion of the life cycle (see Rohde, 1971). Monogeans, gyrocotylideans, and amphilinideans are associated primarily with vertebrates, although at least one species of amphilinidean has an intermediate arthropod host (see Rohde and Georgi, 1983). Both digeneans and eucestodes have, with few exceptions, life cycles involving both an invertebrate and a vertebrate host. For reasons elucidated in the discussion we consider the digenean life cycle to involve secondary addition of a vertebrate host, and the eucestode life cycle to involve secondary addition of an invertebrate host. o. NERVOUS SYSTEM: Monogeneans, gyrocotylideans, amphilinideans, and eucestodes have doubled nervous commissures at the anterior and posterior ends of the body (see Tower, 1900; Watson, 1911; Lynch, 1945; Rohde, 1968, 1975; Allison, 1980; Fairweather and Threadgold, 1983). All other taxa in the study group have single anterior and posterior commissures, as do all rhabdocoels (Bullock and Horridge, 1965). p. INVAGINATION OF THE POSTERIOR ADHESIVE ORGAN: Gyrocotylideans, amphilinideans, and eucestodes exhibit partial to complete invagination of the posterior adhesive organ when it occurs during ontogeny. This trait appears to be unique to them. q. POLYZOIC BODY: Eucestodes are the only taxon in the study group that may possess a polyzoic body. r. OSMOREGULATORY SYSTEM: Eucestodes are the only members of the study group whose larvae have protonephridia in the posterior half, rather than anterior half, of the body. In addition, whereas adult gyrocotylideans, amphilinideans, and eucestodes possess a reticulate osmoregulatory system, their early ontogenetic stages have paired lateral ducts joining in a posterior vesicle. This latter condition is characteristic of the rest of the study group throughout ontogeny.
s. LARVAL HOOKS ON THE POSTERIOR ADHESIVE ORGAN: Monogeneans have 12-16 hooks, gyrocotylideans 10 equal-sized hooks, amphilinideans six large and four small hooks, and eucestodes six equal-sized hooks. The other groups have no such hooks. Method of character analysis Dalyelloids were chosen as the putative outgroup because of the characters they shared with some members of the study group. This choice agrees with Karling's (1974) cladistic analysis of the Turbellaria. Our cladogram was initially constructed by Hennigian argumentation (Hennig, 1966; see Wiley, 198la), and then checked with WAGNER analysis from the PHYSYS computer program of Drs. J. S. Farris and M. F. Mickevich. Those character series that were entirely within the study group, and thus not amenable to polarization by a taxonomic outgroup (the dalyelloids), were polarized by the functional outgroup method of Watrous and Wheeler (1981); Farris' (1982)expansion of this method was taken into consideration. Diagnoses and keys A phylogenetic analysis produces a cladogram, or a tree diagram, depicting the inferred genealogical relationships of taxa. From this tree, a verbal classification may be constructed. The main purpose of this form of classification is to describe the topology of the tree and the internested monophyletic groups it contains. This isomorphism produces an efficient information storage and retrieval system. Such a classification may be written as a Linnaean hierarchy, and when augmented with character information a diagnosis of sorts is produced. But it is not intended to be a traditional, inclusive diagnosis of the traits of each taxon. It is instead a description of the characters used in the analysis and the hierarchical level at which they are postulated to be synapomorphic. The diagnosis encompasses characters from homologous series that are two-state (the derived state remains a synapomorphy) or multistate (derived state I evolves into derived state II, and thus becomes synapomorphic at one level and symplesiomorphic at another). Hull (1979) and Wiley (198la) have discussed these properties extensively. For example, a traditional "taxon" diagnosis of the Cercomeria would include "gut saccate, bifurcate, or absent." As we show in our results, a cladistic diagnosis separates the plesiomorphy and apomorphy in this statement and diagnoses the Cercomeria as "gut saccate" because that is concluded to be the primitive gut condition. The other two gut characters are introduced at the less inclusive taxonomic levels where they are postulated to have evolved. Cladistic diagnoses are also often inappropriate for immediate use as a key. The important attributes of a key are clarity and convenience to allow rapid identification of specimens. It is in classifications, not keys, that phylogenetic relationships are proposed. Sometimes a key can be both succinct and natural (i.e., it follows the classificatory groupings). But this will be so only when the character series involved are all twostate (e.g., if a saccate gut were primitively present and always present in the Cercomeria). However, the existence of multistate character series (i.e., continuing evolution) usually makes an artificial key (i.e., no evolutionary connotations) preferable.
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Results Figure 1 gives the cladogram representing the best supported phylogenetic hypothesis for the cercomerians, based on 39 characters drawn from the 19 putative homologous series listed above. For reasons given in the discussion, some of the characters and series were not used. The same cladogram is obtained whether one uses dalyelloids as the outgroup or calculates the most parsimonious tree possible regardless of the outgroup (see Farris, 1979). We will show later that the use of acoel turbellarians as an outgroup for some of the members of our study group gives a poorer fit to the data than does our use of rhabdocoels. Numbers accompanying the slash marks on each branch of the cladogram refer to characters that are postulated to be synapomorphic at the level of the branch where they occur. The numbered characters are identified in the classification.
Class Trematoda Rudolphi, 1808 DIAGNOSIS: Cercomeridea with dorsal vagina a Laurer's canal (15), cercomer a sucker (16), and copulatory stylet lost (17). Subclass Aspidocotylea Monticelli, 1892 DIAGNOSIS: Trematoda with vaginal opening lost (18) and ventral sucker modified in adults into ventral adhesive disk (19). Subclass Digenea Van Beneden, 1858 DIAGNOSIS: Trematoda with bifurcate gut (20) and complex life cycle with vertebrate host secondarily acquired (21). Class Cercomeromorphae Bychowsky, 1937 DIAGNOSIS: Cercomeridea with armed cercom- er (22), doubled cerebral commissures (23), and doubled posterior commissures (24).
Classification and cladistic diagnosis for the subphylum Cercomeria Brooks, 1982 Subphylum Cercomeria Brooks, 1982 DIAGNOSIS: Rhabdocoelous platyhelminths with no vagina (1), single ovary and paired testes (2), paired lateral excretory vesicles (3), doliiform pharynx (4), saccate gut (5), copulatory stylet (6), no locomotor cilia in adults (7), Mehlis' gland (8), and posterior adhesive organ formed by an expansion of the parenchyma into an external pad, called a cercomer (9). All associated with at least one host type.
Subclass Monogenea Car us, 1863 DIAGNOSIS: Cercomeromorphae with paired lateral vaginae (25), bifurcate gut (26), and 1216 hooks on larval cercomer. Subclass Cestodaria Monticelli, 1891 DIAGNOSIS: Cercomeromorphae with osmoregulatory system becoming reticulate in later ontogeny (27), no intestine (28), posterior body invagination (29), no copulatory stylet (30), cercomer reduced in size and partially or totally invaginated (31), male genital pore not proximate to uterine opening (32), and vestigial oral structures (33).
Superclass Temnocephalidea Benham, 1901 DIAGNOSIS: Cercomeria with anterior tentacles (10). Ectoparasites or commensals of invertebrates.
Infrasubclass Gyrocotylidea Poche, 1926 DIAGNOSIS: Cestodaria with rosette at posterior end (34) and ten equal-sized hooks on larval cercomer.
Superclass Udonellidea Ivanov, 1952 DIAGNOSIS: Cercomeria with genital pores in anterior half of body (11) and vagina (12). Ectoparasites of arthropods.
Infrasubclass Cestoidea Rudolphi, 1808 DIAGNOSIS: Cestodaria with vagina and male genital pore proximate (35) and cercomer totally invaginated (36).
Superclass Cercomeridea taxon novum DIAGNOSIS: Cercomeria with genital pores in anterior half of body (11), vagina (12), male genital pore and uterus proximate (13), and oral sucker (14). Ecto- and endoparasites of vertebrates, invertebrates, or both.
Superorder Amphilinidea Poche, 1922 DIAGNOSIS: Cestoidea with uterine pore in anterior half of body and genital pores in posterior half (37) and with six large and four small hooks on larval cercomer. At least one species known with complex life cycle with invertebrate host secondarily acquired.
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Figure 1. Cladogram representing the hypothesized phylogenetic relationships of the parasitic platyhelminth taxa examined. Characters are denoted by numbered slash marks and identified in the diagnoses in the text. Each slash mark postulates a synapomorphy, or evolutionary novelty, common to all the taxa above that branch. In some cases subsequent evolution has modified the character, creating an homologous, or transformation, series. There are 41 postulated changes for 39 characters indicating two cases of parallel evolution: loss of copulatory stylet (#17 and #30) and acquisition of bifurcate gut (#20 and #26). The taxa are identified as having life cycles that are direct in an invertebrate host (DI) or vertebrate host (D V) or complex with both an invertebrate and vertebrate host (CB) (see text for comments on the life cycles of amphilinideans).
Superorder Eucestoda Southwell, 1930 DIAGNOSIS: Cestoidea with polyzoic body (38), complex life cycles with invertebrate host secondarily acquired (39), protonephridia in posterior half of larva (40), cercomer lost during ontogeny (41), and six hooks on larval cercomer.
Artificial Key for the Subphylum Cercomeria Brooks, 1982
la. Platyhelminths with double nervous
commissures at the anterior and pos-
terior ends of body; larvae with hooks
on the posterior adhesive organ
Class Cercomeromorphae . . . 2
b. Platyhelminths with single nervous
commissures at the anterior and pos-
terior ends of body; larvae without
hooks on the posterior adhesive organ
5
2a. Cercomeromorphae in which the pos-
terior adhesive organ is an opisthap-
tor, bearing suckers and hooks; larval
opisthaptor armed with 12-16 hooks;
direct life cycles; usually ectoparasites
of
fish
Subclass Monogenea
b. Cercomeromorphae with an invagina-
tion at the posterior end of the body
in the adult; gut absent; pharynx ab-
sent; copulatory stylet absent; reticu-
late osmoregulatory system develop-
ing later in ontogeny
Subclass Cestodaria . . . 3
3a. Cestodaria in which the posterior ad-
hesive organ of the adult forms a ro-
sette; larval cercomer with ten equal-
sized hooks; parasitic in Holocephali
Infrasubclass Gyrocotylidea
b. Cestodaria in which the cercomer of the
adult is totally invaginated; vaginal and
male genital pores are proximate
Infrasubclass Cestoidea . . . 4
4a. Cestoidea in which the larval cercomer
has six large and four small hooks;
uterine pore is in the anterior half of
the body, the genital pores are in the
posterior half; parasitic in fish and tur-
tles
Superorder Amphilinidea
b. Cestoidea in which the cercomer is lost
in ontogeny; larval cercomer has six
hooks; adults usually with polyzoic
body; protonephridia in anterior half
of the larvae; complex life cycles
Superorder Eucestoda
5a. Copulatory stylet absent; modified va-
gina forming a Laurer's canal; oral
sucker usually present
Class Trematoda . . . 6
b. Copulatory stylet present; oral sucker
absent
7
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6a. Trematodes in which the posterior adhesive disk is modified to form a large ventral adhesive disc; saccate gut present; direct life cycles; host usually an invertebrate Subclass Aspidocotylea b. Trematodes in which the posterior adhesive organ is a sucker, which can be terminal, midventral, or secondarily lost; gut present, usually bifurcate; complex life cycles; definitive host usually a vertebrate Subclass Digenea 7a. Vagina lacking; genital pores in the posterior half of body; anterior tentacles present (may be secondarily reduced) Superclass Temnocephalidea b. Vagina present; genital pores in the anterior half of body; tentacles lacking Superclass Udonellidea Discussion Character evolution The majority of the characters used in this analysis have been used previously by other workers studying the parasitic platyhelminths. This was done partly to facilitate comparisons with earlier classifications (discussed later), and partly to offer a phylogenetic hypothesis for further comparative work on newer characters. The study by Jamieson and Daddow (1982) on the ultrastructure of platyhelminth spermatozoa appears to be compatible with our analysis, although more work is required (see Rohde, 1971, 1980). Observations on platyhelminth excretory systems by Rohde (1980) and Rohde and Georgi (1983) offer another synapomorphy for the Cercomeridea (flame cell weir apparatus), the Trematoda (lamellated walls in the protonephridial ducts), and the Cestoidea (microvilli in the protonephridial ducts). We must comment on several of the characters we have used, in light of their arrangement on the cladogram. First, we have broadened the use of the term cercomer. This is not simply an a priori decision, but an indication of the homology that we postulate to exist among the posterior adhesive organs of the taxa studied. There are thus two aspects to the matter: the hypotheses of homology drawn from structural studies, and the terms that are used to refer to those structures. The former must have precedence over the latter. Standard usage of the nomenclature would be maintained if the term cercomer was restricted
to the armed posterior adhesive organ found in all larval and some adult cercomeromorphs, the term ventral sucker or ventral adhesive disk was restri cted to the adhesive organs of trematodes, and the term posterior adhesive disk was restricted to the structure found in udonellideans and temnocephalideans. If the posterior adhesive organ of each taxon is given a different name, this can obscure the question of homology, whereas at the same time reinforcing arguments for convergent evolution of holdfast organs. But if all of the posterior holdfast organs of the platyhelminths are derived from a common ancestor, there then exists a multistate homologous series, each of whose characters are synapomorphic at certain levels of the cladogram. If this is the case, then all such organs should have the same name, with appropriate modifiers for further derived states. Character interpretations build cladograms, and cladograms can be used to interpret other characters. We can justify our cladogram in Figure 1 by noting that even if all characters relating to posterior adhesive organs were removed (nos. 9, 16, 19, 22, 29, 31, 34, 36, and 41), the classification would still be fully supported. We can justify our interpretation of the homology of posterior adhesive organs, and our resulting broadening; of the cercomer appellation, by referring to the four basic series of character development in that organ, discussed earlier and summarized in Table 1. Muscularization and hooks appear to be modifications of the phylogenetically earlier posterior parenchymal expansion. We therefore suggest that this expansion be called a cercomer, that modifiers be used to describe further derived states (loculate, sucker, armed, etc.), and that all of the taxa postulated to have inherited it or its modifications be united into a monophyletic group called the Cercomeria. Some recent discussions of cercomeromorph relationships (Llewellyn, 1965;Malmberg, 1974) have placed emphasis on the number and structure of hooks on the larval cercomer. There are four major characters: 12-16 hooks in monogeneans, ten equal-sized hooks in gyrocotylideans, six large and four small hooks in amphilinideans, and six hooks in eucestodes. An initial interpretation from our cladogram would be that of a linear homologous series, from largest number to smallest, indicating an evolutionary trend towards reduction in number of hooks (Fig. 2a). Llewellyn (1965) proposed another se-
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(c) 10
12 - 16 >6 + A
(d) 10
'12 - 16 > 6 >6
Figure 2. Four possible evolutionary transformations for the number of hooks on the larval cercomer in the Cercomeromorphae. All four series fit equally well on the phylogenetic tree in Figure 1 (see text for discussion).
lemnocepholideci
lies (Fig. 2b), suggesting that the four small hooks on the amphilinidean cercomer were secondarily evolved. Malmberg (1974) proposed a series opposite to that of Figure 2a, proceeding from smallest to largest number of hooks. We did not use the larval hooks as characters because we found that a number of different series fit the classification equally well (Fig. 2). That is, they all give equally parsimonious interpretations of the data without the need for postulating parallel or convergent evolution. Mickevich's (1982) Transformation Series Analysis would recognize cercomer hook number as a "trivial" character. This does not mean that it is of no phylogenetic significance, only that current analytic techniques allow too many evolutionary sequences to be considered equally likely. The data cannot be used to choose between hypotheses. One might consider, however, the series in Figures 2b and 2d to be less likely because they require that the four small hooks of amphilinideans be derived from a different embryonic source than the other hooks when no empirical support for this exists. In fact, studies by Malmberg (1974) suggest the opposite, that all larval hooks are homologous. But this is still an open question, pending comparative developmental studies. Regardless of the resolution of this ambiguity, there would still be more than one equally likely series. This character appears at present to be of little help in studies of platyhelminth phylogenetic relationships beyond the recognition that those flatworms possessing an armed cercomer form a monophyletic group. On the other hand, we found that the various characters pertaining to the genital openings in cercomerians provided useful evidence not fully utilized previously. To highlight this, we have
Figure 3. Diagrammatic representation of postulated evolutionary transformations of the relative positions of the genital pores in the Cercomeria. With the exception of the Temnocephalidea, the three pores are the male pore, the vagina, and the uterine pore (see character series k and 1 in Materials and Methods). Temnocephalideans possess a common genital atrium into which open a male canal, a uterine canal, and a canal from the ovary. This last canal functions as both an oviduct and a vagina--functions that become separated in the other taxa with the evolution of a vaginal canal. The anterior end of the diagrammatic bodies is at top. Transformations: (1) pores relocate in anterior, uterine and male pores meet in atrium, vagina ends in parenchyma, opens to dorsal surface, or joins excretory system; (2') uterine and male pores remain together, vagina bifurcates; (2) pores open separately; (3') male pore and vagina relocate in posterior; (3) male pore and vagina meet in atrium, uterine pore remains separate. illustrated the putative homologous series in Figure 3. Previous studies of cercomerian relationships that attempted to link the cercomeromorphs as a group were restricted to one character: the armed cercomer. However, for at least some monogeneans (Rohde, 1968, 1975), gyrocotylideans (Watson, 1911; Allison, 1980), and eucestodes (Tower, 1900;FairweatherandThreadgold, 1983) enough is known of the anatomy of the nervous system to give two additional characters. Digeneans, aspidocotyleans, and all groups of rhabdocoels for which we could obtain data (see Bullock and Horridge, 1965) possess a central nervous system comprised of two bilateral longitudinal trunks with an anterior (cerebral) and posterior commissure. The cercomeromorphs differ in their possession of doubled cerebral and
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posterior commissures. Some eucestodes may even have a third anterior commissure. It was the discovery of doubled posterior commissures in Gyrocotyle that led Watson (1911) to postulate that the eucestode scolex was derived from the posterior end of the body. This theory is falsified by the observation that in gyrocotylideans the rosette develops at the same body end bearing the larval cercomer, whereas in eucestodes (e.g., the cysticercus of Hymenolepis; see Alicata and Chang, 1939) the scolex and cercomer develop at opposite ends of the body. Some ambiguity in character analysis of the nervous system remains, particularly about the condition in amphilinideans, and the differences between ring and bridge commissures (see Lynch, 1945). Our analysis also offers new interpretations of the evolution of the gut in platyhelminths. We have considered three characters: saccate gut, bifurcate gut, and the lack of a gut. Our cladogram in Figure 1postulates that the bifurcate condition is convergent, having evolved separately in the Digenea and Monogenea. The same number of character steps (see the Comparisons with Other Classifications section) results if it is postulated that a bifurcate gut arose once as a synapomorphy for the Cercomeridea, then reverted to a saccate condition in the Aspidocotylea. This alternate interpretation must be considered, especially in view of the existence of aspidocotyleans (e.g., Zonocotyle) with bifurcate guts, and digeneans (e.g., Haplosplanchnidae) and monogeneans (e.g., Bothitrematidae) with saccate guts. These anomalies may be atavistic traits--characters from an earlier phylogenetic position in a homologue series. The likelihood of this is greater when the organisms are one of the most plesiomorphic taxa in their clade. The more derived a taxon is, the more likely it becomes that an apparent atavism is actually a further derived state with superficial similarity to the plesiomorphic state. A cladistic analysis of the Digenea to the family level by Brooks et al. (1985)suggests that haplosplanchnids are a relatively derived taxon and therefore nonatavistic in their gut condition. Similar studies are necessary for the Aspidocotylea and Monogenea before any further conclusions can be made. The third gut character we have examined is that of the lack of a gut. We have suggested that this condition, which occurs in the Cestodaria (sensu nobis), is best interpreted as a derived state within the Cercomeria, rather than evi-
dence that a gut never existed in the ancestors of gyrocotylideans, amphilinideans, and eucestodes (we discuss other authors' hypotheses of an acoel ancestry for the Cercomeromorphae in a later section). Our interpretation of secondary loss can be supported by two lines of evidence. First, those taxa lacking a gut are placed as highly derived groups by synapomorphic characters other than those involving the condition of the gut. All of the cercomerian taxa postulated to be plesiomorphic to the Cestodaria possess a gut. Second, it may not be the case that cestodarians lack any vestige whatsoever of a digestive system (as opposed to a gut). By this we do not refer to the question of the existence of entoderm or entoderm precursor cells in eucestode development (see Mackiewicz, 1981, and references therein). If these are present, there is simply a confirmation of the symplesiomorphic trait of the presence of a gut (with the derived character no. 28 in Fig. 1 becoming "gut components present in ontogeny" instead of "no gut"). But given our first line of evidence above, this a secondary point whose perceived importance to phylogenetic study arises from assumptions of the necessity for recapitulatory ontogeny (as well as assumptions about the formation of germ layers during cestodarian embryogenesis--see below). We refer instead to the question of structures associated with a gut in the more plesiomorphic flatworm taxa. Trematodes and monogeneans exhibit, as do rhabdocoels, a form of ectolecithal embryogenesis (see Hyman, 1951; Rees, 1940). There is no folding of germ layers to form body cavities. Instead, a part of the ectoderm grows inward, then hollows out and forms a mouth (which may become surrounded by an oral sucker) and pharynx invagination, and parts of the parenchyma hollow out and form the intestine. The embryogenesis of the Cestodaria is not so easily categorized, mainly because of changes in the relative sizes of the blastomeres. The basic pattern is nevertheless ectolecithal or hemiectolecithal (see Douglas, 1963, and references therein). Cestodarian embryos clearly do not develop into adults possessing an intestine formed by an internal parenchymal cavitation (the larvae of the Cyclophyllidea possess another cavity, called the primary lacuna [see Freeman, 1973]). They do, however, display, at some stage in ontogeny, an anterior invagination of the ectoderm with varying degrees of muscularization and paren-
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chymal modification. In gyrocotylideans and most amphilinideans this persists throughout life. We have observed living Gyrocotyle in the spiral valve of ratfish using this structure to take in host gut contents. If functional definitions are used, the absence of an intestine precludes calling the anterior invagination a mouth. In gyrocotylideans and amphilinideans it is termed an anterior invagination, and in eucestodes it is called an apical sucker. But, as with existing terminology for posterior holdfast organs, the nomenclature may be obscuring homologies. All of the Cercomeria possess an anterior invagination of the ectoderm at some time in ontogeny, and in all groups except the Cestodaria it becomes a functional pharynx and mouth when it connects with an intestine formed by a parenchymal cavity. Given these observations, we postulate that the anterior invagination of cestodarians is a vestigial mouth, and is therefore evidence of the primitive presence of a complete digestive system. Adaptive significance of characters Under current evolutionary theory, perceptions of the adaptive significance of characters will affect hypotheses of their origin and their relationship to similar characters in other taxa. In the cercomerian nervous system, the doubled commissures can be examined. Although it is relatively easy to envisage plausible functional explanations of what these structures do today, we suggest that there is no adaptive significance in their evolution, that is, the reasons for their appearance in the first place. Digeneans and aspidocotyleans have oral suckers and pharynges that operate with a single cerebral commissure, so the second commissure in monogeneans cannot be an adaptation for oral function. The two cerebral commissures are intimately involved in the development of the eucestode scolex, yet the doubled structure seems to have evolved before either the loss of the gut or the modifications of the mouth and anterior end into a holdfast organ. We interpret this to imply that the doubled commissures first evolved without affecting the functioning of the body ends of ancestral cercomeromorphs. That is, the single commissures in trematodes and the doubled commissures in cercomeromorphs are not only characters in the same homologous series, but functional equivalents (different structures performing the same function) as well.
Adaptationist explanations require either that functional equivalents be nonhomologous (e.g., birds' wings and insects' wings are adaptations for flying but are not homologues; monogenean cercomers and eucestode scolices are adaptations for holding onto the host but are not homologues), or that parts of an homologous series have different functions (e.g., shrew forelimbs are adaptations for burrowing, bat forelimbs are adaptations for flying, yet the two are homologues; monogenean cercomers are adaptations for holding onto the definitive host, eucestode cercomers are adaptations for penetrating the intermediate host, yet the two are homologues). It is undoubtedly the structure of the central nervous system in eucestodes that allows the functioning of the rostellum and four suckers, or of the four bothridia, but that does not mean that the structure is an adaptation for that function (i.e., that it was ever the focus of selection). Gould and Vrba (1982) proposed the term exaptation to refer to structures that arose evolutionarily prior to the time they were coopted by natural selection for a particular function. This term was offered as a refinement of the more general concept of "pre-adaptation." We suggest that there is another way to interpret such character evolution. Some traits may evolve without any functional difference from the ancestral trait, i.e., the two would be functional equivalents. However, these new traits might allow other evolutionary changes to take place, which in turn could have major evolutionary consequences. For example, dalyelloid rhabdocoels kept alive in our laboratory adhere to a substrate by flattening the posterior end of their body and applying their adhesive secretions (an indication that posterior adhesive behavior was present in the outgroup before complex posterior adhesive organs evolved in the study group). With innervation capable of functioning in such a manner, many structural modifications of the posterior end could act as holdfasts. Similarly, the occurrence of doubled anterior nerve commissures would provide the innervation basis for the subsequent evolution of scolices. Our alternate interpretation can also be applied to explanations of the evolution of tegumental structures in the Cercomeria. Finger-like projections of the tegumental surface are especially well developed in those parasitic platyhelminths lacking a gut. This has led to explanations that such structures evolved in order to
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produce an alternative nutrient absorptive surface. But these projections have been found, to one degree or another, in temnocephalideans, trematodes, monogeneans, gyrocotylideans, amphilinideans, and eucestodes (e.g., Lee, 1966, 1972; Williams, 1981; Rohde and Georgi, 1983). They have, in fact, been reported to be present in all platyhelminths (Bedini and Papi, 1974). Lee called all such projections microvilli. Other workers (see Jarecka et al., 1981, and references therein) have adopted Rothman's (1963) distinction between those projections containing only cytoplasm (microvilli) and those with electron-dense caps as well (microtriches). The latter are especially prevalent around the scolex and neck in eucestode adults. Jarecka et al. (1981) demonstrated that although microtriches are present on the necks and scolices of procercoids, cercoscolices, cysticercoids and cysticerci, there are microvilli (sensu Rothman) on the "tails" of procercoids, cercoscolices and cysticercoids, the cyst wall of cysticercoids, and the bladder wall of cysticerci. An intermediate type of projection occurs in gyrocotylideans (Lyons, 1969) and amphilinideans (Rohde and Georgi, 1983). Developmental studies (e.g., MacKinnon and Burt, 1984) on eucestodes indicate that microtriches are derived from microvilli. Other studies suggest that rostellar hooks are derived from microtriches (Mount, 1970). Malmberg (1974) (see Fig. 7) noted that tegumental similarities could be the result of (1) convergent evolution in digeneans and cercomeromorphs, with parallel evolution within the Cercomeromorphae (a postulate that is more parsimoniously interpreted to be a synapomorphy); or (2) the result of a common ancestor for digeneans and cercomeromorphs. Rohde and Georgi (1983) considered the projections in amphilinideans to be an adaptation to food absorption and of "no great phylogenetic significance" (but see Rohde, 1980). We suggest that not only are digitiform tegumental projections in the Cercomeria homologous, but that their functional utility in cestodarians is a consequence of their primitive occurrence in platyhelminths with a gut, which allowed the survival of descendants lacking a gut. No postulates of convergent or parallel evolution are necessary. The evolution of life cycles Our classification allows some hypotheses to be formed about the origin of life cycles in the
Cercomeria (see also O'Grady, 1985). The life cycle criteria for the nine taxa can be mapped onto the cladogram in Figure 1 as direct life cycles involving invertebrate or vertebrate hosts, or complex life cycles involving both invertebrates and vertebrates. A direct cycle in an invertebrate is concluded to be plesiomorphic because it is the life cycle of the most plesiomorphic taxa. This conclusion is reached by both direct inspection of the taxa and Farris optimization (Farris, 1970) of the nodal values. The questions asked are (1) in what manner did a direct cycle in a vertebrate arise, and (2) are the complex cycles of digeneans and eucestodes (as well as some species of amphilinideans) an example of convergent evolution? Certainly the life cycles in the Digenea and Eucestoda appear functionally similar, with larval stages developing in invertebrates and the adults in vertebrates. In each case, a dissemination of life stages results. Differences arise, however, when the morphological traits and sister-group relationships are examined. In eucestodes, it is the larvae that bear the closest resemblance to the adults of the sistergroups, the Amphilinidea, Gyrocotylidea, and Monogenea. The armed cercomer, for example, synapomorphic for the Cercomeromorphae, is present in only the early developmental stages of eucestodes. These include the hexacanth, procercoid, cysticercoid, and exceptionally the cysticercus (see Jarecka, 1975, Fig. 4). The characters representative of most eucestodes, such as a scolex and polyzoic body, are best interpreted as adult characters added to the end of the ancestral developmental sequence by terminal addition. Furthermore, whereas adults of other members of the Cercomeromorphae develop in invertebrate hosts, the comparable (i.e., of the same phylogenetic origin) developmental stage in eucestodes--the larva--develops in a more recently acquired invertebrate host. Because this relatively newer host harbors an intermediate developmental stage, its means of acquisition is one of intercalation, or nonterminal addition to the ancestral direct life cycle in vertebrates. Rohde and Georgi's (1983) discovery that Austramphilina elongata develops through an intermediate arthropod host indicates that the life cycle changes hypothesized above may actually be synapomorphic for the Cestoidea. The study by Janicki (1928) on Amphilina foliacea indicates this as well (see Rohde and Georgi, 1983). The data in Figure 1 suggest that the evolution
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of the life cycle in digeneans occurred in a reverse manner to that of eucestodes. Adult digeneans most closely resemble the adults of their sistergroups, the Aspidocotylea, Udonellidea, and Temnocephalidea. For example, these groups possess an unarmed cercomer (as defined earlier), synapomorphic for the Cercomeria. The only nonadult digenean stages to have this structure are the cercariae and metacercariae. The larval stages associated with the complex life cycle-- miracidia, sporocysts and rediae--lack this character and do not appear to have comparable developmental stages in the most closely related taxa. This suggests an intercalation of developmental stages by nonterminal addition. With respect to the hosts, adults of dalyelloids, temnocephalideans, udonellideans, and aspidocotyleans develop in association with invertebrates (some aspidocotyleans occur with vertebrates). In digeneans, this plesiomorphic host group contains the relatively new larval stages, whereas the plesiomorphic developmental stage, the adult, is found in the more recently acquired vertebrate host. This acquisition is best interpreted as a terminal addition to the ancestral life cycle. Our analysis therefore suggests that the complex life cycles of digeneans and eucestodes evolved by different means. 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. Vertebrates also appear to have been colonized by the ancestral cercomeromorphs. A number of general conclusions are implied by this hypothesis. First, as with morphological characters, Hennigian analysis allows life cycle components to be treated as composites of plesiomorphic and apomorphic states, inherited and modified at different times. It is not necessary to search for the "archetypal" digenean or eucestode. Second, the term "complex life cycle" is too broad to be applied to both the Digenea and Eucestoda when evolutionary conclusions are to be drawn from the comparison. Third, the terms "intermediate host" and "definitive host" may
have two meanings. One is functional, the other is historical. Our study has shown that the functional usage may obscure evolutionary differences. The historical usage, however, does not obscure the functionality of the hosts. Thus, we would call the plesiomorphic host for digeneans (the mollusc) thefunctional intermediate host and the plesiomorphic host for eucestodes (the vertebrate) the functional definitive host. This retains information about both the history and the function of the taxa involved. Comparisons with other classifications Previous classifications for these platyhelminths include those by Spengel (1905), Janicki (1920), Fuhrmann (1928, 1931), Bychowsky (1937, 1957; see also Beklemishev, 1969; Dubinina, 1974), Llewellyn (1965), Price (1967), and Malmberg (1974). For reasons we will discuss later, it is difficult to make comparisons with the work of Spengel and Janicki. The classifications of the remaining authors are presented in Figures 4-9, rendered in a form comparable with our results. Numbers accompanying the slash marks refer to the characters from our cladogram in Figure 1, optimized with Farris' (1970) method in order to obtain the best fit possible. In some cases this resulted in hypotheses of evolution and inclusion of groups which the original author did not suggest, but with which a better fit to the stated hypotheses could be obtained. We have thus attempted to ensure that differences result from the classifications themselves and not from differential treatment of the data. At the same time we recognize that by adding data to an earlier classification we are not examining that proposal exactly as its originator formulated it. For systematics, however, these concerns are superseded by the necessity to treat every classification as an hypothesis subject to testing with new information. Classifications can be assessed in two ways. The first is the efficiency with which the data are described. This amounts to postulating the least amount of homoplasy or minimizing the type 2 ad hoc assumptions discussed earlier. Homopla-
Figures 4-9. Cladograms depicting previous classifications of the parasitic platyhelminths, and the postulations of character evolution they require. Numbered slash marks refer to characters in Figure 1, "X" indicates an evolutionary reversal. Branches ending in a node (rather than a terminal taxon) that bear no slash marks propose a grouping that has no character support.
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Figures 4-6. 4. Fuhrmann (1928, 1931). 5. Bychowsky (1937, 1957). 6. Llewellyn (1965). Copyright © 2011, The Helminthological Society of Washington
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8 PRICE (1967) 9 PRICE (1967) Figures 7-9. 7. Malmberg (1974). 8. Price (1967) (phylogenetic tree). 9. Price (1967) (classification). Copyright © 2011, The Helminthological Society of Washington
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sy shows up in two ways in the classifications. These are: (1) postulations of parallel or convergent evolution, tabulated by counting the number of duplicated numbers on the trees; and (2) postulations of evolutionary reversals, or the secondary loss of a trait, tabulated by counting the number of characters denoted by an "X" on the trees. The fewer of either of these, the better the summary of the data. Efficiency can also be measured by the consistency index (CI) of Kluge and Farris (1969). This is calculated by dividing the minimum numbers of steps needed to represent the data (i.e., each character evolves once) by the actual number of steps required to support a particular classification. The closer the CI is to 1.0, the better the fit of the data to the tree. Our classification, for example, has a minimum number of 39 steps (39 characters), and an actual number of 41 steps, giving a CI of 39/41, or 0.95. The departure from maximum efficiency comes from the postulation of two cases of homoplasy: the loss of a copulatory stylet in the Trematoda and Cestodaria, and the development of a bifurcate gut in the Digenea and Monogenea. The second way in which classifications can be assessed is by examining them for groupings of taxa for which there are no distinguishing characters; that is, the branch uniting those taxa on the tree has no character support (slash marks in Figs. 4-9). This can result from a type 1 ad hoc assumption, discussed earlier, in which taxa of secondary importance in a study group are grouped together by default because they do not possess a structure that has been used to highlight the taxa of primary interest (see Price, 1967, on the Acercomeromorphae). An unsupported grouping can also be included in a classification for heuristic, rather than empirical, reasons (see Inglis, 1983, on the Aschelmintha). Clearly, it is not helpful for taxonomic groupings to be devoid of diagnostic features; nevertheless, a number of higher taxa have been defined by what they are not. For example, "reptiles" are amniotes without bird-like or mammal-like features; the reptiles as a group have no distinguishing traits. Inspection of a phylogenetic tree for the Tetrapoda shows that reptiles are not an evolutionary group (Wiley, 1981b), that is, not all reptiles are each others' closest relatives. Birds and crocodiles (the Archosauria) are more closely related to each other than they are to any other group of organisms. Portions of classifications, therefore, that have empty branches when represented as a phy-
Table 2. Comparisons of previous classifications of parasitic platyhelminths with the present study. Three criteria are used to evaluate the fit of the classifications to the data set of 39 characters in Figure 1: the efficiency of character representation (number of steps), the degree to which the classification is supported by ambiguous characters [the consistency index, or CI, of Kluge and Farris (1969)--see text], and the number of unsupported groupings (number of empty branches). A good fit to the data is indicated by a high CI and a low number of steps and empty branches. Two of the four empty branches in Llewellyn's classification come from the postulation of paraphyly in the Eucestoda.
Author Fuhrmann, 1928,1931 Bychowsky, 1937, 1957 Llewellyn, 1965 Price, 1967 (tree) Price, 1967 (classification) Malmberg, 1974 Present study
No. of steps 46 55 59 43 50 50 41
No. of empty CI branches
0.85
2
0.71
2
0.66
4
0.91
0
0.78
2
0.78
2
0.95
0
logenetic tree may be suspected of postulating artificial, nonevolutionary groups. Parenthetically, the extent to which such artificial groups have been defined by functional criteria is the extent to which departures from a strictly phylogenetic classification have been justified by reference to adaptive scenarios. Table 2 summarizes the step length, CI, and empty branch statistics for the classifications we examined. Those by Fuhrmann (1928, 1931), Llewellyn (1965), Bychowsky (1937, 1957), and Malmberg (1974) appear to have made unnecessary postulates of convergent evolution. Such empirically unjustified departures from the data are difficult to detect when they can be considered to support perceptions of the adaptive plasticity (i.e., capacity for homoplasious evolution) of parasites (e.g., Price, 1980). The classification by Malmberg (1974) is especially interesting because it is the only explicit, rather than anecdotal, attempt to support the hypothesis that cercomeromorphs are more closely related to acoel turbellarians than they are to trematodes. A review of this hypothesis is beyond the scope of this paper; it has gained recent support from Malmberg (1974), Logachev and Sokolova (1975), Freeman (1982). and Mackiewicz (1981,1982). Its basic argument cites the absence of a digestive system in cestodarians (sensu nobis). Malmberg (1974) stated:
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"If the absence of mouth, pharynx and intestine in the ontogeny of cestodes, the amphilinideans and the gyrocotylideans implies that these body parts were never evolved here, then these groups cannot have originated from rhabdocoelan creatures." Freeman (1982) gave the most succinct statement of the evidence: "Incidentally not even the suggestion of endoderm let alone a tube-like gut in the ontogeny of any present-day cestode (e.g. see Logachev and Sokolova, 1975), suggests that it never had such a g u t . . .." We are dissatisfied with this type of reasoning. It is not possible to decide, by reference to a character's absence alone, whether that condition is due to primitive absence or subsequent loss (i.e., whether it is a primitive or derived character). Other characters must be examined. We suggest that the perceived necessity for all ancestral characters to remain in a descendant's ontogeny comes from perceptions of the ubiquity of recapitulatory development and evolution by nothing but terminal addition of developmental stages. The necessity of corroborative characters, however, may be a moot point in this case, in light of our earlier suggestion that the anterior invaginations of cestodarians may be vestigial mouths and pharynges. Malmberg (1974) recognized the problems that secondary loss and expectations of recapitulatory development could create for phylogenetic studies, but his proposed solution--the primitive absence of a gut in the cercomeromorphs--creates problems of another sort. Let us assume for the sake of argument that anterior invaginations in cestodarians are convergent traits having nothing to do with a gut. There are still 38 other characters to be explained. Confirmation of the primitively gutless nature of cestodarians could come from those other characters analyzed independently. But, as we have shown, the most efficient and least ad hoc interpretation of those other characters supports relationships with the trematodes, udonellideans, temnocephalideans, and rhabdocoels--not the acoels. Malmberg's scheme (Fig. 7) requires 9 cases of convergent evolution to account for the structural similarities among the parasitic platyhelminths that we include in the Cercomeria. Karling (1974), in a cladistic analysis of the
Turbellaria, considered trematodes and cercomeromorphs to be derived from rhabdocoels. Also, platyhelminths may not be primitively gutless at all. The Cnidaria, Ctenophora, Gnathostomulida, and Nemertinea, as well as most platyhelminths, have intestines. Even some acoels, such as Nemertoderma, have intestines (see Karling, 1967). If the cercomeromorphs are grouped with acoels, on the basis of their gutless condition alone, there are still some gutless platyhelminths excluded from that grouping. Some dalyelloid rhabdocoel (Fecampiidae) parasites of crustaceans, such as Kronborgia amphipodicola, have no mouth, pharynx, or intestine (Christensen and Kanneworff, 1964). Levenseniella (Monarrhenos) capitanea is a microphallid digenean that lacks a pharynx and has only a few fibrous intestinal tissues (Overstreet and Perry, 1972). Clearly, one does not classify these taxa with the cercomeromorphs and acoels. Such a decision would require the postulation of a very large amount of homoplasious evolution of rhabdocoel-like and digenean-like traits. Our hypothesis of the phylogeny of the cercomeria is an attempt to maintain consistency in the method of inference of genealogical relationships, namely, to apply parsimony considerations to character analysis at every level of generality in the study group. We do not believe that previous classifications can offer adequate justification for the departures from parsimony that some of their groupings require. The classifications by Spengel (1905) and Janicki (1920) are too incomplete to be fully compared with ours. We have attempted an analysis of Fuhrmann's work even though it is only slightly more complete. Spengel and Janicki considered four taxa: rhabdocoels, digeneans, monogeneans, and eucestodes. Spengel's placement of these four corresponds not only to ours, but also to almost every other classification we have considered. Our analysis of Bychowsky's classification, which is an expansion of Spengel's, shows that subsequent taxa and data were interpreted in a suboptimal manner. Janicki's classification was connected with his cercomer theory. He proposed that monogeneans arose from rhabdocoels, then gave rise to digeneans, which gave rise to eucestodes. This interpretation was supported by the conclusion that (1) the cercomer of procercoids, the cyst and tail of cysticercoids, and the bladder of cysticerci are homologues; (2) these are homologous with
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the opisthaptor of monogeneans; and (3) these are homologous with the tail of digenean cercariae. Janicki termed these cercomer-homologue-bearing taxa the "Cercomeromorphae." Bychowsky removed the Digenea from this grouping and retained the term to denote those platyhelminths with an armed cercomer. We have used the term in Bychowsky's sense but altered the inferred relationships of the taxa involved (cf. Figs. 1and 5). Jarecka et al. (1981) drew from earlier work by Jarecka (e.g., 1975) and suggested that the presence of microvilli on the posterior body expansions of eucestode larvae provided support for Janicki's postulates of cercomer homology with the exception of the Digenea. Freeman (1973) noted the importance of distinguishing between the cercomer and the midbody of eucestode larvae when examining such homology. We have offered evidence for extending the series of cercomer homologues first to the trematodes (on the basis of the ventral adhesive disk, rather than the cercarial tail)--to form the Cercomeridea, and then to the Temnocephalidea-- to form the Cercomeria. A third problematic classification is that by Price (1967), who presented both a phylogenetic tree and a classification (see Table 2). The tree is not resolved at its base and is ambiguous as to the monophyly of the Cercomeria. Price's discussion, however, suggests that monophyly was being postulated. If we assume this, his tree can be represented by Figure 8. It differs from ours in two ways. First, it places Udonella in a trichotomy (three branches arising from one node) with trematodes and cercomeromorphs. Second, it does not distinguish between dalyelloid and temnocephalid turbellarians. This creates a problem for the mapping of characters 7, 8, 9, and 10 (see Fig. 1). We think it best, and fairest, to minimize the number of steps by maintaining Price's Turbellaria category, and simply note that not all of its members possess characters 7, 8, and 9, or 10. New problems arise when the phylogenetic inferences of Price's classification are made explicit by converting it into a tree (Fig. 9). The result gives a poorer fit to the data than does his original phylogenetic tree. The classification is therefore inconsistent with the original tree (see Wiley, 198 Ib). This means that the evolutionary relationships it implies are not the same as those given by the tree from which it was constructed. This is caused by the creation of a type 1 ad hoc grouping--the Acercomeromor-
phae. This grouping may have some "pragmatic" utility for the recognition of flatworms whose larvae do not possess an armed cercomer, but given the phylogenetic tree whose relationships the classification is intended to communicate, this trait cannot be considered to be an indicator of monophyly, as can an armed cercomer in the Cercomeromorphae. Conclusions Based primarily upon characters previously used to classify parasitic platyhelminths, we have derived a classification that best fits the data. It embodies elements common to most earlier proposals, and some aspects of each previous classification agree with ours. In total, however, neither our classification nor its justifications have been presented before. Some characters used previously are concluded to be too ambiguous for phylogenetic inference. Others, notably genital pores, posterior adhesive organs, and anterior invaginations are each united into homologous series. Revised terminology is proposed for the latter two character series. The sequence of origin for some traits previously taken to be of special taxonomic importance is considered to be inconsistent with explanations that they evolved as adaptations for a particular function. The classification indicates that the plesiomorphic life cycle of the Cercomeria is direct and in an invertebrate. Vertebrates appear to have been colonized, twice: by the Digenea and by the ancestral cercomeromorphs. Invertebrates, especially arthropods, appear to have been recolonized by the Eucestoda or possibly the Cestoidea. The functional terms of "complex life cycle," "intermediate host," and "definitive host" obscure phylog;enetic relationships. The postulate that cestodarians and monogeneans are descended from acoel turbellarians is rejected on the basis that it derives its support from unjustified assumptions of convergent evolution. The present study also offers new character analyses that conflictwith this hypothesis. The evidence presented herein links monogeneans and cestodarians with trematodes and these three groups with dalyelloid rhabdocoels. Acknowledgments Funds for this study were provided through a grant (A7696) to DRB from the Natural Sciences and Engineering Research Council of Canada (NSERC). ROG thanks NSERC for postgraduate
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support. DRG thanks the University of British Columbia for fellowship support. Susan Bandoni offered useful comments on character analysis. Ms. Maggie Hampong prepared the diagrams. We have profited from discussions with various colleagues and a number of referees. Errors of interpretation rest solely with us. Literature Cited Alicata, J. E., and E. Chang. 1939. The life history of Hymenolepis exigua. J. Parasitol. 25:121-129. Allison, F. R. 1980. Sensory receptors of the rosette organ of Gyrocotyle rugosa. Int. J. Parasitol. 10: 341-353. Bedini, C., and F. Papi. 1974. Fine structure of the turbellarian epidermis. Pages 108-147 />zN. J. Riser and M. P. Morse, eds. Biology of the Turbellaria. McGraw-Hill, New York. 530 pp. Beklemishev, W. N. 1969. Principles of the Comparative Anatomy of Invertebrates. (English translation of 1964 Russian edition, by Z. Kabata.) Oliver and Boyd, University Press, Aberdeen. Vol. 1, 490 pp.; Vol. 2, 529 pp. Brooks, D. R. 1977. Evolutionary history of some plagiorchid trematodes of anurans. Syst. Zool. 26: 277-289. . 1978a. Systematic status of proteocephalid cestodes from reptiles and amphibians in North America with descriptions of three new species. Proc. Helminthol. Soc. Wash. 45:1-28. . 1978b. Evolutionary history of the cestode order Proteocephalidea. Syst. Zool. 27:312-323. . 198la. Revision of the Acanthostominae (Digenea: Cryptogonimidae). Zool. J. Linn. Soc. 70:313-382. . 1981b. Classifications as languages of empirical comparative biology. Pages 61-70 in V. A. Funk and D. R. Brooks, eds. Advances in Cladistics. Vol. 1. New York Botanical Garden, New York. 250 pp. . 1982. Higher level classification of parasitic platyhelminths and fundamentals of cestode classification. Pages 189-193 in D. F. Mettrick and S. S. Desser, eds. Parasites--Their World and Ours. Elsevier Biomedical, Amsterdam. 465 pp. , and J. N. Caira. 1982. Atrophecaecum lobacetabulare n. sp. (Digenea: Cryptogonimidae: Acanthostominae) with discussion of the generic status of Paracanthostomum Fischthal and Kuntz, 1965 and Ateuchocephala Coil and Kuntz, 1960. Proc. Biol. Soc. Wash. 95:223-231. -, T. R. Platt, and M. H. Pritchard. 1984. Principles and Methods of Phylogenetic Systematics: A Cladistics Workbook. Spec. Publ. No. 12 Mus. Nat. Hist., Univ. Kansas. 92 pp. --, M. A. Mayes, and T. B. Thorsen. 198la. systematic review of cestodes infecting freshwater stingrays (Chondrichthyes: Potamotrygonidae) including four new species from Venezuela. Proc. Helminthol. Soc. Wash. 48:43-64. --, R. T. O'Grady, and D. R. Glen. 1985. Phylogenetic analysis of the Digenea (Platyhel-
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Lynch, J. E. 1945. Redescription of the species of Gyrocotyle from the ratfish, Hydrolagus colliei (Lay and Bennett), with notes on the morphology and taixonomy of the genus. J. Parasitol. 31:418-446. Lyons, K. M. 1969. The fine structure of the body wall of Gyrocotyle urna. Z. Parasitenkd. 33:95109. Mackiewicz, J. S. 1981. Caryophyllidea (Cestoidea): evolution and classification. Pages 139-206 in W. H. R. Lumsden, R. Muller, and J. R. Baker, eds. Advances in Parasitology. Vol. 19. Academic Press, London. 225 pp. . 1982. Parasitic platyhelminth evolution and systematics: perspectives and advances since ICOPA IV, 1978. Pages 179-188 in D. F. Mettrick and S. S. Desser, eds. Parasites--Their World and Ours. Elsevier Biomedical, Amsterdam. 465 pp. MacKinnon, B. M., and M. D. B. Burt. 1984. The development of the tegument and cercomer of the polycephalic larvae (cercoscolices) of Paricterotaenia paradoxa (Rudolphi, 1802) (Cestoda: Dilepididae) at the ultrastructural level. Parasitology 88:117-130. Malmberg, G. 1974. On the larval protonephridial system of Gyrocotyle and the evolution of the Cercomeromorphae (Platyhelmithes). Zool. Scripta 3: 65-82. Mickevich, M. F. 1982. Transformation series analysis. Syst. Zool. 31:461-478. Mount, P.M. 1970. Histogenesis of the rostellar hooks of Taenia crassiceps (Zeder, 1800) (Cestoda). J. Parasitol. 56:947-961. O'Gra.dy, R. T. 1985. Ontogenetic sequences and the phylogenetics of parasitic flatworm life cycles. Cladistics. (In Press) Overstreet, R. M., and H. M. Perry. 1972. A new microphallid trematode from the blue crab in the northern Gulf of Mexico. Trans. Am. Microsc. Soc. 91:436-440. Price, C. E. 1967. The phylum Platyhelminthes: a revised classification. Riv.Parassitol. 28:249-260. Price, P. W. 1980. Evolutionary Biology of Parasites. Princeton Univ. Press, Princeton, New Jersey. Rees, G. 1940. Germ cell cycle of the digenetic trematode Parorchis: Part II. Structure of the miraciduum and germinal development in the larval stages. J. Parasitol. 32:372-391. Rohde, K. 1968. Das Nervensystem der Gattung Polystomoides'WaTd, 1917 (Monogenea). Z. Morphol. Okol. Tiere 62:58-76. . 1971. Phylogenetic origin of trematodes. Parasitol. Schriftenr. 21:17-27. . 1975. Fine structure of the Monogenea, especially Polystomoides Ward. Pages 1-33 in B. Dawes, ed. Advances in Parasitology. Vol. 13. Academic Press, London. 277 pp. . 1980. Some aspects of the ultrastructure of Gotocotyla secunda and Hexostoma euthynni. Angew. Parasitol. 21:32-48. -, and M. Georgi. 1983. Structure and development ofAustramphilina elongata Johnston, 1931 (Cestodaria: Amphilinidea). Int. J. Parasitol. 13: 273-287. Rothnian, A. H. 1963. Electron microscopic studies oif tapeworms: the surface structures of Hymeno-
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lepis diminuta (Rudolphi, 1819)Blanchard, 1891. Trans. Am. Microsc. Soc. 82:22-30. Sinitsin, D. F. 1911. Partenogeneticheskoe pokilenie trematod i ego potomstvo v chernomorskikh molliuskakh. Mem. Acad. Imp. Sc. St.-Petersb., Cl. Phys.-Math. 8. s. 30:1-205. Spengel, J. W. 1905. Die Monozootie der Cestoden. Z. Wiss. Zool. 82:252-287. Stevens, P. 1980. Evolutionary polarity of character states. Ann.Rev. Ecol. Syst. 11:333-358. Tower, W. L. 1900. Nervous system of the cestode Monezia expansa. Zool. Jahrb. Anat. 13:359-384. Watrous, L. E., and Q. D. Wheeler. 1981. The out-
group comparison method of character analysis. Syst. Zool. 30:1-11. Watson, E. E. 1911. The genus Gyrocotyle, and its significance for problems of cestode structure and phylogeny. Univ. Calif. Publ., Zool. 6:353-468. Wiley, E.G. 198 la. Phylogenetics: The Theory and Practice of Phylogenetic Systematics. Wiley-Interscience, New York. 439 pp. . 1981b. Convex groups and consistent classifications. Syst. Hot. 6:346-358. Williams, J. B. 1981. Classification of the Temnocephaloidea (Platyhelminthes). J. Nat. Hist. 15: 277-299.
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