Phylogeny of platyhelminthes, with special reference to parasitic groups

International Journalfor Printed in Great Brirain

Parasitology

Vol. 20, No. 8, pp. 979-1007,

1990 0

002~7519/90 $3.00 + 0.00 Pergamoil Press pk Sociefyfor Paresitology

1990 Ausmdian

INVITED REVZEWARTZCLE PHYLOGENY

OF PLATYHELMINTHES, WITH SPECIAL REFERENCE TO PARASITIC GROUPS K. ROHDE

Department of Zoology, University of New England, Armidale, New South Wales 2351, Australia (Received 15May 1990) CONTENTS INTRODUCTION METHODS USED TO STUDY PHYLOGENETIC RELATIONSHIPS The four schools of classification Weighting of characters and criteria of homology A critical examination of characters used to study platyhelminth phylogeny Molecular methods in phylogenetic studies NON-CLADISTIC SYSTEMS OF THE PLATYHELMINTHES A numerical system Systems largely or entirely based on life-cycle data SYSTEM OF PLATYHELMINTHES BASED ON SSrRNA SEQUENCES SYSTEMS BASED ON PHYLOGENETIC SYSTEMATICS (CLADISTICS) Ehlers’ system of the Platyhelminthes Brooks et d’s system of the parasitic Platyhelminthes A system of the Platyhelminthes based on characters likely to be homologous THE PHYLOGENY OF SMALL PLATYHELMINTH TAXA EVOLUTIONARY TRENDS IN THE PLATYHELMINTHES AN ALTERNATIVE HYPOTHESIS: MOSAIC EVOLUTION? SUGGESTIONS FOR FURTHER RESEARCH ACKNOWLEDGEMENTS REFERENCES

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INDEX KEY WORDS: Platyhelminthes; Turbellaria; Aspidogastrea; Trematoda; Monogenea; Cestoda; Amphilinidea; Gyrocotylidea; phylogeny; evolution; cladistics; phylogenetic systematics; phenetics; numerical taxonomy; molecular phylogeny; homology; convergent evolution; mosaic evolution.

INTRODUCTION phylogeny of Platyhelminthes has been discussed by a number of earlier authors (e.g. Hyman, 1951; Ax, 1961, 1963; Beklemischev, 1963; Ivanov & Mamkaev, 1973) largely on the basis of light-microscopic morphology and, to a lesser degree, development. Recent ultrastructural studies and a much more thorough knowledge of life cycles and development of many species have made the older views partially obsolete. Therefore, they will not be discussed here. Emphasis is on the phylogeny of the major groups of parasitic Platyhelminthes, but free-living taxa will be considered as well since an understanding of the phylogeny of free-living groups is essential for an understanding of that of the parasitic ones, especially in view of the fact that some THE

authors have claimed separate origins of various groups of parasitic from free-living platyhelminths. Thus, Malmberg (1974) and Logachev & Sokolova (1975) suggested that cestodes are primarily without an intestine and have arisen from acoel-like ancestors, Llewellyn (1986) claimed separate origins for the digeneans on the one hand and the monogeneans and cestodes on the other, and Cannon (1986) tentatively suggested separate origins of various major taxa of parasitic Platyhelminthes from different families of Dalyellioida. Furthermore, many of the ‘turbellarian’ groups contain a few or many parasitic species. Since references are often scattered in non-parasitological journals not easily accessible to many parasitologists, and since recent reviews of several 979

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aspects are not available, reference to original papers will frequently be made. However, instead of quoting older papers extensively, I shall refer to the major monograph by Ehlers (1985a) and some reviews on more special aspects. A very brief review of the phylogeny of marine helminths including the platyhelminths was recently given by Bray (1986). METHODS

USED TO STUDY PHY LOGENETIC RELATIONSHIPS

The four schools of classzjication Ridley (1986) has discussed the four ‘schools’ of classification, i.e. evolutionary taxonomy, phenetic taxonomy, phylogenetic systematics (cladism in Ridley’s terminology, see Hennig, 1950, 1957, 1966, 1982, 1984; Wiley, 1981; Ax, 1984), and transformed cladism. Evolutionary taxonomy distinguishes homologies and analogies and represents both the order of splitting and phenetic divergence in evolutionary hierarchies. However, both can be in conflict when phenetic change is rapid or convergent, and the decision whether to represent phenetic or phylogenetic relationships is subjective. Phenetic taxonomy, likewise, is subjective because similarity between species depends on the statistics used to measure it. Phylogenetic systematics uses synapomorphies (shared derived characters) in order to classify the order of branching of taxa, assuming the validity of evolution. Transformed cladism uses cladistic techniques but denies their phylogenetic justification. Ridley gives convincing reasons for its rejection. In particular, it uses practical techniques without valid reasons. I follow Ridley in accepting that phylogenetic systematics (cladism) is the most justifiable approach. Unfortunately, however, many so-called cladistic classifications are not truly cladistic but a statistical evaluation of superficial similarities (phenetics), since homologous characters are not thoroughly distinguished from analogous (convergent) ones. Various authors have pointed out that ultrastructural studies, in addition to light-microscopic ones, are useful for phylogenetic considerations (e.g. Rieger, 1981; Starch & Welsch, 1989) and several authors (e.g. Ax, 1984; Watrous & Wheeler, 1981) have discussed the important outgroup comparison, a cladistic method based on the assumption that among alternative character traits found in a presumably monophyletic taxon, the one also occurring outside the taxon is likely to be the plesiomorphic one. Weighting of characters and criteria of homology Recently, several attempts have been made to evaluate weighting procedures in cladistic analysis (e.g. Neff, 1986; Bryant, 1989; Rodrigo, 1989). Neff (1986) distinguished a priori and a posteriori weighting procedures. The former is a procedure logically (not necessarily temporally) prior to the

formation of any groups based on the characters being weighted, the latter “is generated from some criterion logically dependent on the group delineations determined in the same analysis from the characters subject to weight”. Neff concluded that a priori weighting is the only non-circular approach to character weighting. She proposed an objective method for weighting which does not attempt to weight intrinsic properties of characters (such as complexity and presumed likelihood of processes generating a feature, see Bock, 1977), but uses the “relative degree of corroboration of the character in the character analysis”. Rather than asking “how reliable is the character?‘, we can more usefully ask “how reliable is our hypothesis of homology for the character?’ With regard to the complexity of characters she points out that “just because a character is complex does not mean that all the evidence from the complexity will be corroborating. But if all of the evidence from that complexity is thoroughly examined, and it is amply corroborative, then the result is a strong character hypothesis to which greater weight in the analysis should be given.” The answer to Neffs question “How much do we think we know about this character?“, in my opinion, must be based on a thorough understanding of the concept of homology as originally defined in classical comparative anatomy. According to Hillis (1987), “Theoretically, it is possible to weight characters in combined data sets according to their complexity or probability of evolving, but in practice this is largely a subjective procedure”. This is certainly correct, but can be overcome, at least to a certain degree, by a thorough application of homology and functional criteria, as discussed in the following. Homology can be defined as the similarity of structures in space and time due to common ancestry (e.g. Rieger & Tyler, 1985, see also 1979). Similarities not due to common ancestry are convergent traits. Rieger & Tyler have stressed that a structural analysis should be supported by a functional analysis, since the latter can provide arguments against convergence of certain characters, and a structural analysis supplementing a functional analysis can provide arguments against common ancestry. Criteria used for recognizing homologies were discussed in detail by Remane (1952), Riedl (1975, 1978), and Ruppert (1982). Rieger & Tyler summarized them as follows: (1) homologous structures (in space and time, i.e. morphological structures, physiological and behavioural processes, etc.) have a similar position relative to other structures in an organism, as well as similarities in the position of substructures; (2) even dissimilar characters may be homologous if they are connected by a (usually temporal) sequence of intermediate forms (ontogenetic or morphological sequence); (3) structures can be interpreted as homologous if their distribution in a group of organisms coincides with other similarities. The first criterion is the most important and should always be

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FIG. 1. Diagrams of flame bulb and protonephridial capillary of Trematoda Aspidogastrea, Trematoda Digenea and Monogenea. A. Longitudinal section through flame bulb. B, C. Cross-sections through capillary. D. Cross-section through weir. Note septate junction (sj), internal (il) and external leptotriches (el), internal (ir) and external ribs (er) connected by a ‘membrane’ (m), cytoplasmic cords (cco), lamellae (1) and reticulum (r) of capillaries, cilia (c) of flame arising from terminal cell (tc), vesicles (v) and nucleus (n) of terminal cell. Scale bars = 1 pm.

used first. Aspects of functional analysis were discussed by Remane (1952) Riedl (1962, 1966, 1975, 1977) and Tyler (1988). Criteria for a functional analysis were suggested by Rieger & Tyler (1985) as follows: (1) the suspicion that similar structures are due to convergence rises with increasing correlation between the similarity of structures and certain environmental conditions; (2) the probability of convergence is inversely correlated with the number of ‘solutions’ to a certain

problem; (3) different ontogenetic origins of structures suggest convergence; (4) the occurrence of a common (similaritydependent) selection pressure (e.g selection pressure for co-evolution) suggests convergence. The first two criteria, according to Rieger & Tyler, are the most important. It must be stressed that decisions about homologies are probability decisions or, in the words of Ruppert (1982), “homologies are hypotheses, not demonstrated

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FIG. 2. Diagrams of flame bulb and protonephridial capillaries of cestodes. A. Longitudinal section through flame bulb. B. Cross-section through capillary. C. Cross-section through weir. Note lack of cytoplasmic cords in weir, lack of septate junction along flame bulb and capillary, and presence of short microvilli (mv) in capillaries. Note cilia (c), external ribs (er), internal leptotriches (il), internal ribs (ir), ‘membrane’ (m), nucleus (n) and terminal

cell (tc). Scale bar = 1 pm.

facts”, and that synapomorphies used in phylogenetic systematics (cladistics) must be homologous (Hennig, 1950, 1966). A critical examination of characters used to study platyhelminth phylogeny In the following, I examine some structures used for constructing phylogenies of Platyhelminthes, in the light of the above discussions on character weighting and homology criteria. An important structure in several classifications of

the Platyhelminthes is the pharynx. Thus, Ehlers (1984a,b, 1985a) established the taxon Doliopharyngiophora for those groups thought to have a doliiform pharynx, and the supposed close relationship between the Neodermata and Dalyellioida is largely based on the supposed similarity of the pharynges (e.g. Hyman, 1951: “the digestive system” of the trematodes “closely resembles that of the dalyellioid rhabdocoels”). Evidence is practically non-existent. Only two ultrastructural studies of the pharynges of Neodermata have been published, those of Rohde

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FIG. 3. Diagrams of flame bulb and protonephridial capillary of Udonella. A. Longitudinal section through flame bulb. B. Cross-section through capillary. C, D. Cross-sections through weir. Note cilia (c) of flame and internal leptotriches (il) arising from terminal cell (tc), internal (ir) and external ribs (er) connected by a ‘membrane’ (m), large cross-striated rootlets (cr) of cilia. some basal bodies Cbb) scattered in cvtonlasm of terminal cell, nucleus (n) of t&&nal cell, mitochondria (mij, aid numerous desmosomes (d) at base of weir. Scale bar = lpm.

(1974, 1986~) on three species of Monogenea, and very few ‘turbellarians’ have been thus examined (references in Rohde, 1986~). Joffe & Chubrik (1988) and Joffe, Slusarev & Timofeeva (1987) made detailed light-microscopic studies of the pharynges of 11 species of Trematoda and seven species of Monogenea, respectively, and concluded that they are more similar to the pharynges of the Typhloplanoida (with a rosulate pharynx) than to those of the Dalyellioida (with a doliiform pharynx). But even these similarities

have to be substantiated by electron-microscope studies to exclude the possibility of convergent evolution in the Typhloplanoida and Trematoda/Monogenea. Joffe (1987), on the basis of light-microscopic studies of the pharynges of various flatworms, concluded that the relative position of muscle layers in the pharynx walls, particularly of the Neoophora, is a constant feature of higher taxa and may be of phylogenetic significance. He further concluded that a doliiform pharynx has evolved repeatedly in

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FIG. 4. Diagrams of flame bulb and capillary of Temnocephalida. A. Surface view. B. Longitudinal section through flame bulb. C. Cross-section through capillary. D. Cross-section through weir. Note branching and interconnected external leptotriches (el), microtubules (mt) in longitudinal ribs (r), ribs forming a single row, ‘membrane’ (m) between ribs, and dense cytoplasm (dc) lining the lumen of the capillary. Scale bars = 1 pm.

different groups including the parasitic ones, and that the latter have not evolved from the polyphyletic Dalyellioida. Similarly, there is no evidence whatsoever (either light- or electron-microscopic) that the posterior adhesive organ in Udonellidea, Temnocephalidea and Monogenea/Cestoda is homologous (see also Lebedev, 1988), as claimed by some authors. All we know is that animals attaching themselves to hosts have discs or suckers for attachment, which in the Monogenea/Cestoda bear hooks. Detailed morphological studies of the tissue composing the organs in and possibly studies of their all these groups, development, would be necessary to justify homologization. Strong selection pressure towards more effective attachment in all these groups could easily have led to convergent evolution of sucker-like structures. In contrast to our meagre knowledge of posterior attachment organs, the protonephridial system has been studied by electron microscopy in many taxa of free-living and symbiotic flatworms, as well as in other lower invertebrates. It is among the best known organ system of the flatworms and its homology

within various groups is well supported by many ultrastructural observations, of which only some examples will be discussed. (1) (1st homology criterion) In all the Neodermata (major groups of parasitic Platyhelminthes), the weir of the protonephridium is formed by two rows of longitudinal ribs connected by a ‘membrane’ of extracellular matrix, the inner ribs continuous with the terminal, the outer ones with the proximal canal cell (Figs. l-3); the Trematoda and Monogenea have, in addition, two longitudinal cytoplasmic cords continuous with the proximal canal cell and connected by a septate junction (Fig. 1, references in Rohde 1988, 1989b); all ‘turbellarian’ Rhabdocoela, i.e. the Dalyellioida, Temnocephalida, Kalyptorhynchia and Typhloplanoida, have a weir, formed by a single cell, with a single row of longitudinal ribs containing bundles of microtubules (Fig. 4, references in Rohde, Watson & Cannon, 1987, and Rohde, Cannon & Watson, 1988~). (2) (3rd homology criterion) A septate junction along the protonephridial capillaries and lamellae and/or a reticulum of spaces in the wall of the capillaries are present in the Trematoda/Monogenea

Phylogeny of Platyhelminthes (Fig. l), whereas a continuous wall of the capillaries and short microviili are present in the cestodes (Fig. 2) coinciding with the distribution among taxa of a certain type of weir (references in Rohde, 1989b).

Furthermore, the Neodermata, besides a similar flame bulb, also share a similar type of spermatozoan (two axonemes of the 9 + ‘1’ type incorporated in the sperm body), a tegument (= neodermis) connected to subtegumental perikarya by branching cytoplasmic processes, and sense receptors with electrondense collars (references in Ehlers, 1985a; Rohde, 1988). (3) (1st functional criterion) The same type of weir is found in ectoparasitic Monogenea on the gills of freshwater and marine fish (Rohde, 1980, 1982, 1989~; Rohde, Justine & Watson, 1989; Rohde, Watson & Roubal, 1989a), in endoparasitic Monogenea in the urinary bladder of turtles (Rohde, 1973b, 1975) in free-living larvae of digenean trematodes (Kiimmel, 1958; Pan, 1980) and in adult digeneans from the liver of vertebrates (e.g. Jeong, Rim, Kim, Kim & Yang, 1980), etc., in larval aspidogastreans from freshwater and marine molluscs and in adults from the intestine of marine fish and freshwater turtles (Rohde, 1971c, 1972a, 1982, 1989b). A different type of weir is found in ‘turbellarian’ Rhabdocoela free living in freshwater and marine habitats (Rohde, Watson & Cannon, 1987; Rohde, Cannon & Watson,

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1988c), as well as symbiotic on freshwater crayfish (Rohde, 1986a, 1987b; Rohde, Cannon & Watson, 1988~). (4) (2nd functional criterion) Many ‘solutions’ to ‘constructing’ the terminal parts of the protonephridia in Platyhelminthes and related lower invertebrates are known. In the Tricladida, weirs have rows of short ‘fenestrae’ (three species examined, references in Rohde, Watson & Sluys, in press); Catenulida have a terminal cell with two cilia, whose elongate rootlets extend along the weir, and some species have a weir consisting of an outer layer of transverse and inner layer of longitudinal ribs (Kiimmel, 1962; further references in Ehlers, 1985a); in the macrostomid Paromalostomum proceracauda the ‘terminal complex’ of the protonephridium consists of three cells, each with a separate weir but with a common weir lumen (Brtlggemann, 1986b); the prolecithophoran (?) Urastoma cyprinae has a system of rods coiled around each other (Rohde, Noury-Sraiii, Watson, Justine & Euzet, in press), etc. (for other lower invertebrates see, for example, Brandenburg, 1962, 1966, 1970, 1975; Teuchert, 1967, 1973; Lammert, 1985). (5) (3rd functional criterion) Ultrastructural observations of the amphilinid Austramphilina elongata and light-microscopic observations of several species of Cestoidea have shown that cytoplasmic cylinders

FIG. 5. Diagrams of flame bulb and capillary of Mono&is (Proseriata). A. Surface view. B. Longitudinal section through flame bulb. C. Cross-section through capillary. D. Cross-section through weir. Note septate junction (sj) along flame bulb and capillary, internal leptotriches (il) and cilia (c) arising from terminal cell (tc), ‘membrane’ between internal (ir) and external ribs (er), cytoplasmic cord (cco) along weir, and lamellae and reticulum (r) of capillary. Also note cells with nuclei (n) tightly surrounding the flame bulb. Scale bars = 1 pm. Modified according to Rohde, Cannon & Watson (1988b).

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of a single proximal canal cell enclose flames of three terminal cells during ontogeny (Rohde & Watson, 1988a; Bugge, 1902) indicating the same ontogenetic origin of the weir at least in the cestodes. (6) (4th functional criterion) Trematodes endoparasitic in the intestine of vertebrates have a weir with two longitudinal cytoplasmic cords connected by a septate junction, as characteristic of all Trematoda and Monogenea from any habitat (e.g. Rohde, 1971c, 1989b), whereas cestodes in the same habitat have a weir without such cords (e.g. Swiderski, Euzet & Schonenberger, 1975) as characteristic of all cestodes from any habitat, i.e. a common selective pressure has not led to similar protonephridia (further references in Rohde, 1989b). In summary, the homology of the terminal parts of the protonephridia, i.e. the flame bulbs, between the various taxa of Trematoda and Monogenea, between those of the Amphilinidea, Gyrocotylidea and Cestoidea, and between those of various ‘turbellarian’ Rhabdocoela is so well supported that great weight must be given to it in establishing phylogenetic systems. Also likely, but to a somewhat lesser degree, is the homology of the terminal parts of the protonephridia between taxa of Trematoda-Monogenea and Cestoda, and between those of the ‘turbellarian’ Rhabdocoela (with microtubules in the ribs) and the lecithoepitheliate Prorhynchidae (e.g. Timoshkin, Mamkaev & Osipova, 1989; but without microtubules, unpublished observations). Also likely is the homology of the flame bulbs of the proseriate Monocelis (Fig. 5, see Rohde, Cannon & Watson, 1988b) and, to a lesser degree, that of at least some Macrostomida (Steiner, K., unpublished B. SC. Honours thesis, University of New England, 1987), and possibly Prolecithophora (see Rohde, Noury-Srai’ri, Watson, Justine & Euzet, in press) with those of the Neodermata. In addition to the protonephridia, the following characteristics of the Neodermata are very likely to be homologous. A ciliated larval epidermis cast off at the end of the free-swimming life and replaced by a syncytial neodermis (tegument) connected to subtegumental perikarya by branching cytoplasmic processes is found only in the Neodermata (references in Ehlers, 1985a). Epidermal locomotory cilia, with a single horizontal rootlet as characteristic of Neodermata (references in Ehlers, 1985a), occur sporadically in some species of ‘Turbellaria’ (e.g. in the umagillid Seritiu stichopi, see Rohde, Watson & Cannon, 1988c) but are almost certainly due to convergent evolution (in view of the different structure of other features). Electron-dense collars of sense receptors, found in all Neodermata examined to date, also sporadically occur in ‘Turbellaria’ (e.g. Sopott-Ehlers, 1984; Rohde, Cannon & Watson, 1988a) but they have a different structure and location within the receptor. Two axonemes of a 9 + ‘1’ pattern, completely incorporated in the sperm

body, are known also from Kalyptorhynchia, but, in view of fundamental differences in other features, must be considered to be the result of convergent evolution (references in Ehlers, 1985a). At the level of smaller taxa, Udonellu has a sperm identical to that of certain Monogenea (Justine, Lambert & Mattei, 1985) although the ultrastructure of the flame bulb (Rohde, Watson & Roubal, 1989b) clearly indicates that it is not a monogenean (Rohde, Watson & Roubal, 1989a; Rohde, Justine & Watson, 1989). Studies of spermiogenesis may show that it differs from that of Monogenea. Altogether, ultrastructure of mature sperm should be weighted less than, for example, ultrastructure of flame bulbs, at the level of smaller taxa. Features listed as apomorphies for various smaller taxa of Neodermata will not be discussed in detail, but those listed as a basis for my phylogenetic system (see below) are very likely homologous, in view of their restriction to particular taxa and (in many cases) their complex structure. In particular, the ventral adhesive disc, microtubercles of the tegument (neodermis), and the septate oviduct clearly are synapomorphic homologues of the Aspidobothrea (besides several other traits, at least of the Aspidogastridae). Concerning the non-parasitic Platyhelminthes (references in Ehlers, 1985a) the structure of the epidermal locomotory cilia (bend of main ciliary rootlet, system of rootlets connecting cilia, sharp shelf in distal part of cilia) very likely is a synapomorphy of the Acoelomorpha, in view of its complexity and uniqueness. Similarly, the structure of the ciliary rootlets of each group of Acoelomorpha is unique to the group, very complex and therefore likely to be apomorphic to each group. Lamellar rhabdites and the very complex duo-glandular system consisting of three characteristic cells are synapomorphic for the Rhabditophora (but lost in several ‘higher’ groups). Of great importance is the complex 9 + ‘1’ pattern of the axoneme of sperm of Trepaxonemata (all Rhabditophora except the Macrostomida, which have non-flagellate sperm, probably due to secondary loss). The central axis of the axoneme has a double-helical structure unique among sperm in the animal kingdom (a 9 + 1 structure of sperm axonemes is known from some Acoela, but the central axis has a different structure, see Rohde, Watson & Cannon, 1988a). Molecular methods in phylogenetic studies Hillis (1987) has discussed the relative advantages of morphological and molecular approaches to systematics and concluded that a combination of both can maximize information content and usefulness. According to him, the greatest advantage of molecular data is the extent of the data set, andwhereas few morphological characters are shared among major groups of organisms-biomolecules provide a phylogenetic record across the whole

Phylogeny of Platyhelminthes organismic realm. Ghiselin (1988) stressed that some molecules evolve relatively independently of the rest of the body and are unlikely to undergo extensive convergence or parallelism, although this is not necessarily so and different molecular methods do not always give strictly consistent results. Molecular analysis can be applied to systematics at different levels. Since mtDNA (mitochondrial DNA) of eukaryotes contains some of the most rapidly evolving DNA sequences, studies of these have been useful for examining differences between populations of a species and other closely related organisms (e.g. Moritz, Dowling & Brown, 1987). Allozymes have been similarly used. Ribosomal RNA (rRNA), on the other hand, evolves very slowly (see Ghiselin, 1988) and is therefore useful for detecting phylogenetic relationships at a higher level. Other DNA sequences have intermediate evolutionary speeds (see Olsen, 1988). Restriction enzyme mapping of ribosomal DNA has been used to distinguish species of one genus (e.g. Fasciola, see Blair & McManus, 1989) and DNA x DNA hybridization (e.g. Sarich, Schmid & Marks, 1989) has given good results for relatively small taxa but not between phyla. Studies using SSrRNA have been used to construct a phylogenetic system of most organisms, from cyanobacteria to Metazoa (Hori & Osawa, 1986, 1987) and also of the Metazoa (Hendriks, Huymans, Vandenberghe & de Wachter, 1986; Hori, Muto, Osawa, Takai, Lue & Kawakatsu, 1988). However, SSrRNA contains only about 120 nucleotides, rather small for phylogenetic studies, and the results of Hori and co-workers are therefore open to some doubt, since there is practically no overlap between the ‘lowest’ and ‘highest’ species even within the Metazoa, and since some obviously natural groups are broken up by trees based on these data (e.g. Cavalier-Smith, 1989). 18rRNA, on the other hand, contains approximately 1800 nucleotides, sufficient for most phylogenetic work (Ghiselin, 1988). The disadvantage of the latter is the lack of a large data base, whereas SSrRNA data are available for many animal species. For phylogenetic studies of the various taxa of Platyhelminthes, the variable region of approximately 140 base pairs named ‘V3’ seems appropriate. Very small samples can be sequenced using the polymerase chain reaction (PCR, see Mullis & Faloona, 1987). NON-CLADISTIC SYSTEMS OF THE PLATYHELMINTHES A numerical system Bazitov (1984) used the presence or absence of 43 characters and the optimization algorithm of Smirnov (1969, cited in Bazitov, 1984) modified by Tamarin (1972, cited in Bazitov, 1984) to calculate relationships between the various taxa of parasitic Platyhelminthes (Fig. 6). Characters used include, for example, (excretory system) “terminal cells with

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FIG. 6. Phylogenetic relationships of major groups of parasitic Platythelminthes according to Bazitov (1984). Modified from Bazitov (1984).

many bundles of cilia”; (structure of larval stage) “ciliated epithelium”; “ciliated membrane” or “presence of an intestine”, etc. Recent ultrastructural data, for example on the larval epidermis, or the excretory system, are not taken into account, and an evaluation of the homology of characters in different taxa is not made. Hence, the approach is a pheneticnumerical one which I do not accept as valid (see above). The superficial similarities result in a network of ‘relationships’ between groups (Fig. 6) of which the Amphilinidea and Cestoda are considered to be the most original, and the Caryophyllida and digenean Trematoda the least original, in contrast to all cladistic systems, which consider the Aspidogastrea/Digenea the most original parasitic taxa. Systems largely or entirely based on life-cycle data An early discussion of life histories and systematics of Platyhelminthes is given by Stunkard (1975). Llewellyn (1986) assumed, on the basis of studies of life-cycle stages, that digenean trematodes and ‘oncophoreans’ (= monogeneans plus cestodes) had separate origins. Both groups, originally, had direct life cycles, digeneans parasitizing molluscs and oncophoreans vertebrates. The miracidium of digeneans was unarmed, whereas the oncophorean oncomiracidium had 16 marginal hooks. In each line a second host was acquired accidentally, in the early digeneans through the free-living adult being ingested, and in oncophoreans through the eggs of endoparasitic ‘protocestodes’ being ingested “and hatching to release hooked larvae in the gut of a range of microphagous animals”. Pressure in both groups to improve the efficiency of transfer between hosts led to the evolution of cysts in digeneans, and to the incorporation of a further predator first serving as a paratenic, then as a facultative and finally as an obligatory host in the cestodes. The life cycle of Gyrocotyle is a ‘probable (though yet to be established)’ single-host one, and thus, “gyrocotylideans may be regarded as endoparasitic monogeneans which have lost their gut”.

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There are many objections to Llewellyn’s hypothesis. In particular, Xylander (1989) has given a number of reasons why Gyrocotyle probably has an indirect life cycle (even the smallest worms from chimaeras already have an anterior invagination; young chimaeras feeding on yolk are not infected, infection appears to be connected with ingesting certain food items; free larvae are active swimmers and have well developed nerves and receptors, apparently needed to infect an intermediate host). More generally, Llewellyn completely ignores ultrastructural evidence which clearly shows that all major groups of parasitic Platyhelminthes are closely related. Thus, ultrastructure of the flame bulbs, etc. in trematodes and monogeneans is identical, indicative of a common ancestor of the two taxa. Llewellyn argues against a common ancestor of the Neodermata by asking “what were the neodermatan incipient oncophoreans doing in the period (many millions of years?) during which their sister-group digeneans were developing their association with molluscs and before vertebrates became available hosts to both digeneans and monogeneans?” Here, the possibility of a host switch is not considered nor our ignorance concerning exactly when present host taxa first became infected. Llewellyn’s conclusions seem to be supported by Lyons (1966) who has provided evidence for the similar chemical nature of attachment sclerites of Monogenea and other platyhelminths, and concluded that the findings “helped to substantiate the view” that the cestodes and monogeneans are more closely related to each other than to the digeneans. However, this conclusion is difficult to accept since digeneans do not have posterior attachment sclerites. Furthermore, the affinity of monogenean hook protein with vertebrate keratins may indicate a strong selection pressure and/or physiological constraints leading to chemically similar structures in unrelated taxa. Cannon (1986) tentatively proposed some possible relationships between various symbiotic Turbellaria and the major groups of parasitic Platyhelminthes, although he stressed that the origins of the parasitic flatworms are obscure and that “direct lineages are unrealistic”. According to him, the Digenea/Aspidogastrea may be related to the Graffillidae, the Monogenea either to the Dalyelliida/Temnocephalida/ Udonellida or the Umagillidae/Acholadidae/Sterastericolidae, and the cestodes to the Fecampiidae. Evidence given is similarity in ‘lifestyle trends’, particularly the host infection site and certain morphological traits connected with the particular way of symbiosis. Cannon’s scheme cannot be accepted, because a cladistic approach using homologies has not been used (all similarities between groups are superficial, likely to be due to convergent evolution). Furthermore, separate origins of different groups of parasitic platyhelminths from different turbellarian ancestors have to be rejected on the basis of ultrastructural evidence. The occurrence of a single horizontal rootlet in locomotory epidermal cilia in the

umagillid Seritia stichopi, resembling the rootlets of Neodetmata, is almost certainly due to convergent evolution; other umagillids have either a vertical plus horizontal rootlet as characteristic of other ‘turbellarian’ rhabdocoels, or the vertical rootlet is rudimentary (Rohde & Watson, 1988b; Rohde, Watson & Cannon, 1988~). SYSTEM OF PLATYHELMINTHES

BASED ON

SSrRNA SEQUENCES

The only phylogenetic studies using rRNA of platyhelminths are by Hori et al. (see above). A polyclad and a freshwater planarian were found to be ‘completely different’, separated by nematodes and located lower in the phylogenetic tree than Porifera and Cnidaria. This conflicts with trees based on morphology and must be doubtful since SSrRNA with few nucleotides was used (see above). SYSTEMS BASED ON PHYLOGENETIC SYSTEMATICS

(CLADISTICS)

Ehlers’ system of the Platyhelminthes The most detailed phylogenetic system of all the Platyhelminthes is by Ehlers (1984a,b, 1985a,b, 1986) based on a thorough review of the literature and many new ultrastructural data (Fig. 7). Ehlers accepts Ax’s (1984, 1985) view that the sister group of the Platyheiminthes is the Gnathostomuhda, both forming the taxon Plathelminthomorpha, which in turn is the sister group ofall other Bilateria, i.e. the Eubilateria. On this basis, Ehlers (1985a) defines the following autapomorphies for the Platyhelminthes (called Plathelminthes by him); (1) epidermal cells moderately multiciliate (0.2-l .8 cilia pm-’ epidermal surface area); (2) epidermal cilia always without accessory centriole at basal body; (3) two bilaterally symmetrical protonephridia with more than one terminal cell (branching of protonephridial system increases with body size); (4) terminal (and canal) cells of protonephridia not uniciliate, but bicihate, both cilia without accessory centriole and without inner circle of eight supporting microvillus rods; (5) no mitosis of epidermal and other somatized cells (differentiation of new soma cells exclusively from stem cells); (6) formation of a simple copulatory organ and a male genital opening (both characters perhaps already present in the stem line of the Plathelminthomorpha). A cladogram redrawn and modified from Ehlers (1985a) is given in Fig. 7. The slash-marks and numbers refer to the putative autapomorphies of each branch. For details of the autapomorphies, the reader is referred to Ehlers (1985a). In the following, I list only some, especially those of special interest to the parasitologist and important for understanding the discussion. The numbers correspond to those in Fig. 7. The Catenulida have an unpaired protonephridium (9) two cilia of the terminal cell of the flame bulb with rootlets extending along the weir, either one row of

Phylogeny of Platyhelminthes

FIG. 7. Phylogeny of Platyhelminthes according to Ehlers (1985a). Slash-marks and numbers refer to autapomorphies of taxa (see text). Each asterisk represents one questionable autapomorphy (see text) (possibly an autapomorphy of another taxon or a convergent character).

longitudinal and one row of transverse ribs, or a single row of longitudinal ribs (lo), and non-ciliate male ‘gametes’ with a lamellar body but lacking a nucleus (12). In the Euplathelminthes, the epidermal cells have a large number of cilia (14) and a frontal organ is present (16). The Acoelomorpha have epidermal locomotory cilia with a complex pattern of ciliary rootlets (17), there is a sharp shelf near the tip of the cilia (18) and protonephridia are absent (19). The Nemertodermatida possess a statocyst with two statolith formation cells (21) whereas the statocyst of the Acoela consists of two wall cells and one statolith formation cell (25). The sperm of Acoela has two cilia (27) and the two axonemes are incorporated in the sperm body (28). Rhabditophora are characterized by lamellar rhabdites (30) and the terminal cell of the protonephridia is multiciliated (32). Mature sperm cells of Macrostomida are non-ciliate (37) whereas the Trepaxonemata have sperm with two cilia (38) and axonemes of sperm with a complex central axis (9 + ‘1’ pattern) (39). Polycladida have a phcate pharynx (41) in the Neoophora, ovary and vitellarium are separate (47) and the egg is ectolecithal (48). The oocytes of Lecithoepitheliata are surrounded by vitellocytes (50). The position of the Taxon N.N.1. is not clear, a possible synapomorphy is, for instance, presence of Mehlis’ gland (52). Prolecithophora have non-ciliate sperm (56) the Taxon N.N.2. consisting of Seriata and Rhabdocoela has only one ‘possible’ synapomorphy, and the pharynx of the Seriata is a pharynx tubiformis (59). The weir of the proto-

nephridia of the Proseriata is formed by two cells (63). Tricladida have a primarily three-branched intestine (64), and the Rhabdocoela are characterized by a bulbous pharynx. No autapomorphy is known for the ‘Typhloplanoida’, presumably a paraphyletic group. A doliiform pharynx (69) characterizes the Doliopharyngiophora, and the ‘Dalyellioida’ are probably paraphyletic. The Udonellida are provisionally included in the ‘Dalyellioida’, but their exact position is unknown, although they probably do not belong to the Neodermata. The Fecampiidae may be the sister group of the Neodermata. In the latter, a ciliated cellular epidermis is cast off at the end of the freeswimming larval phase (71) and replaced by a neodermis connected to subepithelial perikarya by several or many cytoplasmic processes (72). Epidermal cilia of the Neodermata lack a vertical or caudal rootlet (73), receptors have ‘collars’ (74) flame bulbs have two rows of longitudinal ribs formed by a terminal and an adjacent canal cell (75) and the two axonemes are incorporated in the sperm body (76). Autapomorphies of the Trematoda are, among others: presence of a cirrus (79), of the Aspidobothrii a septate oviduct (84), of the Digenea vegetative multiplication in a mollusc host (85) of the Cercomeromorphae presence of caudal hooks (93), of the Monogenea ectoparasitism on a gnathostomous vertebrate and loss of the original invertebrate host (96) and of the Cestoda a syncytial ciliated epidermis with intraepithelial nuclei (97). The Gyrocotylidea have a rosette-like adhesive organ (103) and characteristic

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for the Nephroposticophora is a caudal excretory opening (107). A specific apical organ (110) is found in the Amphilinidea, in the Cestoidea the number of caudal hooks is reduced to six (111) and the larva has neither a nervous system nor epithelial sensory cells (112). The sperm of Caryophyllidea is uniciliate (115), and the six caudal hooks are completely eliminated in the metacestoid stage (120). Some major criticisms of Ehler’s system are as follows (without consideration of the putative sister group of the Platyhelminthes): (1) As pointed out by Smith, Tyler & Rieger (1986) there is no compelling evidence to include the three major groups, Catenulida, Acoelomorpha and Rhabditophora in one phylum, the Platyhelminthes, and Klauser, Smith & Tyler (1986) and Klauser & Tyler (1987) have shown on the basis of ultrastructural and histochemical evidence that the so-called frontal organ of Acoela and Macrostomida, for example, is not homologous (also Smith & Tyler, 1986). Ultrastructural studies of the epidermal cilia of Xenoturbella (see Franz&n & Afzelius, 1987) strongly indicate that the Xenoturbellida should be included as the most original taxon in the Acoelomorpha (see Rohde, Watson & Cannon, 1988b). (2) All the Neodermata have a protonephridial weir formed by two cells, a terminal and a canal cell; such a weir is also found in the Macrostomida and Proseriata, and flame bulbs consisting of two closely aligned cells (although with a different kind ofweir) are also known from a prolecithophoran. ‘Turbellarian’ Rhabdocoela, in contrast, have weirs formed by a single cell (see above). In view of the complexity of the terminal part of the protonephridia, which make

CERCOMERIA FIG. 8. Phylogeny

convergent evolution of the same type unlikely, it seems probable that the Neodermata are not closely related to the ‘turbellarian’ Rhabdocoela and in particular the ‘Dalyellioida’, but have a sister group much ‘lower’ among the Trepaxonemata as also suggested by Joffe (1987) on the basis of lightmicroscopic studies of the pharynx (for a more detailed discussion see below). (3) The ‘doliiform’ pharynx in the various taxa is unlikely to be homologous (Joffe, 1987), and the only other autapomorphy of the Doliopharyngiophora given is the reduction of the duoglandular system. Reduction can easily occur convergently in evolution and is insufficient justification for establishing a large taxon. Brooks et al. ‘s system of the parasitic Platyhelminthes The second detailed phylogenetic system of the symbiotic (parasitic plus commensal) Platyhelminthes was recently proposed by Brooks, O’Grady & Glen (1985a) and Brooks (1989a,b,c). Brooks et al. (1985a) originally based their system exclusively on lightmicroscopic characters. Subsequently, Brooks (1989a, b) added characters derived from the studies of Brooks, O’Grady & Glen (1985b) on Digenea, of Bandoni & Brooks (1987) on Amphilinidea and of Bandoni (1987) on Gyrocotylidea. Some new lightmicroscopic, ultrastructural, developmental and lifecycle characteristics were also added. In the following, I give a cladogram (Fig. 8) and some putative synapomorphies from Brooks (1989b) important for understanding the discussion. For a complete list of characters of each group see Brooks (1989b). Asterisks in Fig. 8 indicate possible homoplasies, numbers in the following discussion correspond to numbers in Fig. 8.

NEODERMATA

of parasitic Platyhelminthes according to Brooks (1989b). Slash-marks and numbers refer to synapomorphies of taxa, each asterisk represents one putative homoplasy (see text). Modified from Brooks (1989b).

Phylogeny of Platyhelminthes Brooks includes the superclass Cercomeria in the subphylum Rhabdocoela sensu Ehlers, and the infraphylum Doliopharyngophora Ehlers. Presence of a doliiform pharynx (4) and the reduction of the dualgland adhesive system in the Cercomeria, according to Brooks, characterize it as a member of the Doliopharyngophora. Some important synapomorphies of the Cercomeria are lack of locomotory cilia in adults (7), presence of a Mehlis’ gland (8) and of a ‘cercomer sensu lato’, i.e. of a posterior adhesive organ formed by an “expansion of the parenchyma into, minimally, an external pad” (9). The mouth is terminal or subterminal (lo), and they have a one-host cycle using arthropod hosts (14). Species of Temnocephalidea have cephalic tentacles (16), the Udonellidea have a secondary protonephridial system of canals and pores (29), and in the Cercomeridea an oral sucker is present (33), the two-host life cycle includes an arthropod and vertebrate host (36), and they are endoparasitic (37). The Trematoda have a dorsal vagina (= Laurer’s canal) (38), lamellae in the protonephridial walls (45), and a mollusc-vertebrate life cycle (47). The Aspidobothrea lack a vaginal opening (48) and an oral sucker (53), and the Digenea have a miracidium (54) with one pair of flame cells (56), a sporocyst (57) and cercaria (58). Species of the Cercomeromorphae are characterized by a cercomer armed with hooks (72), they have doubled cerebral commissures (73) and doubled posterior nervous commissures (74), paired lateral excretory openings (75), and 12-16 hooks on the cercomer (76). The Monogenea have paired lateral vaginae (77), have secondarily lost the arthropod host (80), and are ectoparasitic on vertebrates (81), the last characteristic possibly a homoplasy. The Cestodaria have 10 hooks of equal size (92), and no desmosomes in the first excretory canal cell (96). Gyrocotylidea possess a posterior rosette (99) and lack nuclei in the larval epidermis (108) and multiciliary sense receptors (109). Cestoidea have six large and four small hooks (114), microvilli lining the excretory ducts (115), and the uterine opening of the Amphilinidea is proximal to the vestigial pharynx (123). The body of Eucestoda is polyzoic (124), the cercomer is lost during ontogeny (125), there are six hooks on the larval cercomer (126), and cerebral development is paedomorphic, none seen in larvae (135). I do not wish to discuss all the 135 characters used by Brooks to support the branches in his system. Instead, a few important ones will be discussed to show some errors in the system. Cercomeria: there is evidence that the so-called ‘doliiform pharynx’ (4) of the various groups of Cercomeria is not homologous (Joffe, 1987); a typical Mehlis’ gland (8) has not been shown to occur in the temnocephalids. Cercomeridea: there is no evidence that the oral sucker in the various taxa is a homologous organ (33) (according to J. C. Pearson, personal communication, a true oral sucker is found in digeneans but not in aspidobothreans and monogeneans) (compare struc-

991

ture of ‘oral sucker’ in Polystomoides, see Rohde, 1974, and Digenea). Trematoda: not only the Trematoda but also the Monogenea have lamellated walls in the protonephridia (45) (see Rohde, 1973b, 1980). Aspidobothrea: the vagina is homologized with Laurer’s canal under Trematoda (38), and Aspidobothrea as stated below lack a vaginal opening (48). However, the aspidogastrid Lobatostoma has a dorsal opening of Laurer’s canal (Rohde, 1973a). Cercomeromorphae: there is no evidence that many cercomeromorphans (and the most original ones) have doubled cerebral and posterior commissures of the nervous system (73,74) (this may be an autapomorphy of polystomes, e.g. Rohde, 1975). In his synoptic classification, Brooks (1989b) following Ehlers’ (1984b) includes the superclass Cercomeria in the Rhabdocoela and Doliopharyngophora. However, as will be shown later, there are only superficial similarities between the most original cercomerian taxa in Brook’s system, i.e. the temnocephalids, udonellids and trematodes, with the rhabdocoels, similarities easily explained by convergent evolution. The ultrastructure of the protonephridia shows clearly that ‘Cercomeria’ are not closely related to the ‘turbellarian’ Rhabdocoela (see below). The presence of a posterior adhesive organ in the Cercomeria, again, has no value for establishing phylogenetic relationships because its homology between the major taxa has not been established. It is more likely that similar modes of life (attachment to a host) led to the convergent evolution of adhesive pads. Details of ultrastructure indicate that Temnocephalidea, but not the Neodermata, are related to the ‘turbellarian’ Rhabdocoela (see the ultrastructural studies of Williams, 1975, 1977, 1980, 1981, 1983, 1984; Rohde, 1987a,b; Rohde, Cannon & Watson, 1988~; Rohde & Watson, in press, d,e). O’Grady (1985) examined the phylogeny of life cycles of parasitic Platyhelminthes by superimposing the types of life cycles known for each major taxon on the phylogenetic system by Brooks (1982) and Brooks, O’Grady & Glen (1985a), which is identical with the later one of Brooks (1989b) except for not including the Udonellidea. O’Grady assumes that the Amphilinidea and Gyrocotylidea have direct life cycles in vertebrates, which is not true for the Amphilinidea (see Janicki, 1928; Rohde & Georgi, 1983) and probably not true for the Gyrocotylidea (see Xylander, 1989). Aspidocotylea are said to have a direct life cycle in invertebrates but there are several species which have obligatory molluscvertebrate cycles (Rohde, 1972a, 1973a). Therefore, his conclusions are largely based on erroneous evidence. Brooks (1989b) discussed hosts and life cycles of the various parasitic taxa in view of his phylogenetic scheme. Aspidobothrea are assumed to have acquired chondrichthyan hosts (although non-chondrichthyan gnathostomous vertebrates, i.e teleosts and chel-

992

K. ROHDE

L_______L___f

/

,

I

I 9-12 15 RHABDITOPHORA N-N.2 (=PLATYHELMINTHES?) (=TREPAXONEMATA?) (=NEOPHORA?)

FIG. 9. Phylogeny of Platyhelminthes

RHABDOCOELA ("TYPHLOPLANOIDA" AND "DALYELLIOIDA" INCL. TEMNOCEPHALIDA)

based on characters likely to homologous. synapomorphies of taxa (see text).

onians, are infected as well and both the former and latter are separately listed for the Monogenea). Digenean trematodes, on the other hand, are thought to have non-chondrichthyan hosts, but I and others have recently recovered several species of digeneans from holocephalans, suggesting that digeneans may also have acquired chondrichthyan hosts early in their evolution. A system of the Platyhelminthes based on characters likely to be homologous In the following I present hypothetical schemes for phylogenetic relationships of Platyhelminthes (Fig. 9), in particular the Neodermata (Fig. 10). As putative synapomorphies I list those which are likely to be homologous, partly following Ehlers (1985a). Numbers correspond to those in Figs. 9 and 10. If evidence is insufficient, relationships are left open. There are no convincing synapomorphies for all Platyhelminthes, i.e. the Catenulida, Acoelomorpha and Rhabditophora may be unrelated taxa although further research may find synapomorphies. Catenulida: (1) protonephridium unpaired; (2) two cilia of terminal cell of protonephridium with distally elongate ciliary rootlets supporting narrow side of weir, either one row of longitudinal ribs or one row of

Slash-marks and numbers refer to

transverse and one row of longitudinal ribs. Acoelomorpha: (3) main rootlet of epidermal locomotory cilia with bend, all cilia of an epidermal cell connected by system of rootlets; (4) epidermal locomotory cilia with sharp shelf in distal part due to abrupt termination of microtubule doublets 4-7. Xenoturbellida: (5) epidermal locomotory cilia with two large branches of main ciliary rootlet, and a posterior rootlet. Nemertodermatida: (6) epidermal locomotory cilia with one main and a posterior rootlet. Acoela: (7) epidermal locomotory cilia with one main ciliary rootlet, two lateral rootlets branching off the main rootlet near bend, and posterior rootlet; (8) sperm with two cilia of 9 + 0,9 + 1 or 9 + 2 pattern, two axonemes completely incorporated in sperm during spermiogenesis. Rhabditophora (if further studies should fail to find synapomorphies for all the Platyhelminthes sensu latu, including the Catenulida and Acoelomorpha, the phylum Platyhelminthes would have to be restricted to the Rhabditophora of Ehlers, 1984a, b, 1985a): the major difference between the Macrostomida and the Trepaxonemata is the lack of cilia in the sperm of Macrostomida, almost certainly a secondary reduction and hardly sufficient to separate two major

Phylogeny of Platyhelminthes

993

29-30

32-33

23-24

19-21

[

I 1 l-6 NEODERNATA

18 CERCOMERONORPHAE

22 NEPHREXOZEUKTICA

34-35 31 CESTOIDEA 25-28 NEPHROPOSTICOPHORA CESTODA

FIG. 10. Phylogeny of major groups of parasitic Platyhelminthes based on characters likely to be homologous. Slash-marks and numbers refer to synapomorphies of taxa (see text).

taxa; studies of spermiogenesis of several species of Macrostomida are needed to show whether axonemes of the 9 + ‘1’ pattern are indeed absent; (9) lamellar rhabdites; (10) duo-glandular system consisting of one anchor and two adhesive gland cells; (11) more than two cilia in terminal cell of protonephridia; (12) sperm with two axonemes of 9 + ‘1’ pattern (central rod of complex double-helical structure). Taxon N.N. 1: (13) flame bulb (not necessarily weir) usually formed by two cells (possibly apomorphic for other tubellarians or plesiomorphic). Macrostomida: (14) sperm non-ciliate (secondary loss of cilia). Taxon N.N.2: (15) flame bulb with a single row of longitudinal ribs, formed by a single cell. Neoophora: supposed synapomorphy ectolecithal egg [the validity of this taxon is not clear, it may be a further synonym of the Rhabditophora (?=Platyhelminthes)]. The discussion in Ehlers (1985a) shows that a gonad containing both egg and yolk cells occurs sporadically also in Acoelomorpha, polyclads and macrostomids, and the situation in the Lecithoepitheliata is not clear. Macrostomida appear to always have an ectolecithal egg, even when the female gonad contains vitellocytes, but the ultrastructure of the protonephridia suggests a close relationship of macrostomids with certain neoophorans, e.g. the Proseriata and Neodermata, whereas some neoophorans, e.g. Tricladida and possibly the Polycladida, have a different protonephridium with a weir containing many slits (see below). Presence of an

endolecithal egg in the Macrostomida may therefore be of secondary importance (possibly due to secondary loss of separate yolk cells in the egg). Karling (1940, 1967, cited in Ehlers, 1985a) has suggested that, at least in the polyclads, the female gonad is secondarily simplified from a primarily heterocellular gonad producing both oocytes and vitellocytes. The apomorphies for the Lecithoepitheliata (reduction of duo-glandular adhesive organ, oocytes surrounded by vitellocytes), Prolecithophora (strongly modified sperm with extensive membranous folds derived from mitochondria, non-ciliate, complete reduction of duo-glandular adhesive organ), Proseriata (no lamellate rhabdites, cranial rootlets of epidermal cilia converge and terminate together at cranial margins of epidermal cells), and Tricladida (threebranched intestine, two ovaries at anterior ends of ovovitelloducts) are insufficient to determine the position of the taxa in the system of Platyhelminthes. The similarities of the terminal parts of the protonephridia of Prolecithophora and Proseriata with those of the Macrostomida indicate a close relationship between these taxa. The weir of Tricladida (and possibly Polycladida) containing many slits may be closer to those of the macrostomids, etc. than superficially apparent; studies of its development may clarify this. Neodermata, on the basis of the ultrastructure of the protonephridia, are also close to the macrostomids, etc., whereas the Rhabdocoela including the ‘Typhloplanoida’ and ‘Dalyellioida’, the

994

K.

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latter including the Temnocephalida, have fundamentally different protonephridia formed by a single cell. Prorhynchus, a genus of Lecithoepitheliata, has a flame bulb similar to those of Rhabdocoela but lacks the bundles of microtubules in the ribs of the weir (unpublished observation; also see Timoshkin et al., 1989 for another prorhynchid). On the basis of these considerations, I leave the exact taxonomic position of most of these taxa open, but assume that the Neodermata and at least some of the ‘turbellarian’ taxa (i.e the Proseriata and probably the Prolecithophora) form one lineage, whereas the Rhabdocoela including the Temnocephalidea and perhaps the Lecithoepitheliata form another, having branched off a rhabditophoran ancestor very early. Many of the socalled synapomorphies of the ‘higher’ rhabdocoels, in particular the temnocephalids and the Neodermata, such as a doliiform pharynx (4 of Brooks, 69 of Ehlers), lack of locomotory cilia in adults (7 of Brooks), presence of a posterior adhesive organ (9 of Brooks), of a terminal or subterminal mouth (10 of Brooks) are therefore likely to be due to convergent evolution. This conclusion is supported by the fact that there is no evidence for the homology of the ‘doliiform’ pharynx (see Joffe, 1987) and the posterior attachment organ (see above) of various taxa. The posterior adhesive organ of temnocephalids, udonellids, trematodes and monogeneans shows at best some superficial similarity; detailed ultrastructural studies and studies of the development of these structures have not been made but would be necessary to provide evidence for homology. Loss of structures occurs frequently in evolutionary lines and the lack of cilia is therefore not a convincing synapomorphy; a certain position of the mouth is a direct consequence of the mode of feeding and was probably acquired independently in taxa with similar feeding habits. It is by no means clear that the most original neodermatans were ectoparasites. The trematodes, likely to be such original forms, are endoparasitic (see below). The Fecampiidae, small turbellarians with a ciliated free-swimming larva and adults endoparasitic in marine crustaceans, are sometimes considered to be the sister group of Neodermata. Both taxa have a ciliated epidermis carrying epidermal locomotory cilia with a single horizontal rootlet (larva and female of Kronborgia amphipodicola: Bresciani & Ksie, 1970; Koie & Bresciani, 1973; male of K. isopodicola with vertical and horizontal rootlets: Williams, 1990). Sense receptors lack electron-dense collars as found in the Neodermata (Koie & Bresciani, 1973). Secondary loss of a vertical ciliary rootlet is also known from the Umagillidae (Rohde, Watson & Cannon, 1988~) possibly a result of a parasitic way of life, and may therefore be due to convergent evolution in the Fecampiidae as well. However, Fecampiidae and Neodermata share a second characteristic, complete incorporation of two axonemes of a 9 + ‘1’ pattern in the sperm body (Williams, 1988), known from only some other turbellarians, i.e. the Kalyptorhynchia

(Rhabdocoela). Although convergent acquisition of this last characteristic in the Fecampiidae cannot be ruled out, occurrences of two independent features both in the Neodermata sensu Ehlers and Fecampiidae suggest that they may indeed be sister groups. The Fecampiidae are usually included in the Rhabdocoela. However, since detailed ultrastructural studies of the protonephridia and the larval pharynx and, for comparison, pharynges of various Rhabdocoela have not been made, the exact position of the group must be left open. I include it in my scheme provisionally, as the sister group of the Neodermata, of unknown ‘turbellarian’ affinities. Ultrastructural studies of the protonephridia may show that it should be included in the Neodermata, or alternatively, that similarities between the Fecampiidae and Neodermata are due to convergent evolution. A hypothetical phylogenetic system of the Neodermata is given in the following, proceeding from Ehlers (1984a, 1985a), and to a lesser degree from Brooks (1989a, b) but with strong modifications (Fig. 10). Neodermata: (1) ciliated epidermis cast off at end of free-swimming larval phase and replaced by peripheral syncytium (tegument = neodermis) connected to subsurface perikarya by several cytoplasmic processes; (2) epidermal locomotory cilia with single horizontal rootlet; (3) most sensory receptors with electron-dense collars; (4) weir of protonephridium formed by two rows of longitudinal ribs and two cytoplasmic cords connected by a septate junction, the external ones and the cords continuous with the canal cell, the internal ones with the terminal cell (possibly plesiomorphic); (5) protonephridial capillaries with septate junction(s) and lamellated/reticular wall; (6) two axonemes of 9 + ‘1’ pattern completely incorporated in sperm body. Trematoda: (7) ciliated epidermal cells with intraepithelial nuclei; (8) male copulatory organ is a cirrus; (9) one-host cycle with mollusc host (possibly two-host cycle: mollusc-vertebrate). Aspidobothrea: (10) larva (cotylocidium) with ventrocaudal sucker which develops to a large alveolated adhesive apparatus or a series of suckers in the adult; (11) larva with only few ciliated patches; (12) neodermis with microtubercles; (13) septate oviduct. Digenea: (14) vegetative multiplication in mollusc; (15) ciliated epidermal cells of miracidium in regular transverse rows; (16) two-host life cycle (molluscpossibly already synapomorphy of vertebrate, Trematoda); (17) evolution of dispersal stage: tailed cercaria. Cercomeromorphae: (18) posterior end of larva with hooks. Monogenea: (19) larva (oncomiracidium) with three complexes of ciliated epidermal cells; (20) two pairs of rhabdomeric photoreceptors; (21) one-host life cycle, ectoparasitic on vertebrate, loss of original invertebrate host. Nephrexozeuktica: (22) septate junction and lamella/

Phylogeny of Platyhelminthes reticula of walls of protonephridia and cytoplasmic cords of weir lost. Udonellidea: (23) caudal hooks lost; (24) flame bulb connected to adjacent tissue by numerous desmosomelike structures. Cestoda: (25) ciliated epidermis of larva syncytial, with intraepithelial nuclei; (26) complete reduction of intestine; (27) two-host life cycle [invertebrate (probably crustacean)-vertebrate]; (28) protonephridial capillaries with numerous short microvilli. Gyrocotylidea: (29) posterior rosette organ; (30) anterior proboscis. Nephroposticophora: (31) posterior opening of protonephridial system. Amphilinidea: (32) male and vaginal pores at posterior end, uterine pore at anterior end; (33) uterus N-shaped. Cestoidea: (34) reduction of caudal hooks to six; (34) tegument (neodermis) with microtriches on most part of the body; (35) sperm without mitochondria. The scheme outlined above seems to be the interpretation of available data most likely to be correct. However, it must be kept in mind that the only synapomorphic characteristic of the Udonellidea and Cestoda, i.e. the lack of septate junction in the flame bulb (Figs. 2, 3) may have arisen separately in both groups. If this is the case, udonellids may have a different phylogenetic position, perhaps closer to the root of the Neodermata. Likewise, although it seems improbable, the caudal hooks in the Monogenea and Cestoda may have evolved independently, i.e. there may be two major neodennatan lineages with a common root at the very base of the Neodermata, one characterized by protonephridia with a junction and lamellate/reticulate walls of the capillaries (Trematoda, Monogenea), one without a junction and with short knob-like microvilli in the capillaries (Cestoda). THE PHYLOGENY OF SMALL PLATYHELMINTH TAXA Various authors have attempted to clarify the phylogeny of taxa within each major group of freeliving Platyhelminthes, and between some of the major groups (e.g. Xenoturbellida: Franzen & Afzelius, 1987; Rohde, Watson & Cannon, 1988b; Acoela and Nemertodermatida: Tyler & Rieger, 1975, 1977; Rieger, 1985; Smith & Tyler, 1985; Seriata: SopottEhlers, 1985; Martens & Schockaert, 1988; Tricladida: Sluys, 1989; Temnocephalidea: Williams, 1986; Prolecithophora: Ehlers, 1988). With respect to the parasitic groups, some discussions of cestodes are by Jarecka (1975) Bazitov (1976, 1981) Mackiewicz (1981; further references in Mackiewicz, 1982a,b, 1988) and Hoberg (1989). Ubelaker (1983), on the basis of embryological evidence, postulated that the cestodes have evolved from a sponge-like ancestor and grouped the Amphilinidea and Gyrocotylidea with the Trematoda and Monogenea. Considering the dis-

995

cussion above and in particular the ultrastructure of protonephridia, this view has to be rejected. Phylogenetic studies of trematodes, among others, are by LaRue (1957), Stunkard (1963) Ginetzinskaya (1971) Pearson (1972, in press), Cable (1974, 1982) Clark (1974) and Shoop (1988). Gibson, D.I. (1978. Abstract in Parasitology 77: xxxi, 1981, 1987) based his discussion on life cycle and morphological evidence. Brooks et al. (1985b) used 113 adult and 90 larval morphological characters for a cladistic analysis, later supplemented and updated by Brooks, Bardoni, MacDonald & O’Grady (1989). A historical review of the systematics and evolution of digenean trematodes was given by Odening (1974) and small taxa of Digenea were examined by Brooks (1977,1979, 1980). Gibson, D. I. (1983. Abstract in Parasitology 87: xiii, 1987) Gibson & Chinabut (1984) and Brooks et al. (1989) established a phylogenetic system of the Aspidobothrea (= Aspidogastrea) which will not be discussed in detail here. However, it should be stressed that ultrastructure and life cycles of species in the families Stichocotylidae, Multicalycidae and Rugogastridae have not been studied. Their relationship with the only family which is well known, the Aspidogastridae, therefore remains obscure. The Monogenea are among the better known groups, and a system supported by two independent lines of evidence has been established for them, in parts further supported by earlier evidence. Hence, they will be discussed in somewhat greater detail (for earlier studies see Bychowsky, 1957; Llewellyn, 1970, 1981; Gussev, 1978). Lambert (1980a,b) established a system based largely on the chaetotaxy (distribution patterns of sensilla) and ciliated patches of the larva, the oncomiracidium (Fig. 11). Justine, Lambert & Mattei (1985) used detailed comparative studies of the ultrastructure of sperm for their system (Fig. 12) which shows close similarity with Lambert’s scheme. A major difference is the position of the Gyrodactylidae, which are included in the Polyopisthocotylea by Lambert but, according to Justine et al. belong to the Monopisthocotylea. Furthermore, Udonella is not considered by Lambert, but thought to be close to the Gyrodactylidae and Euzetrema by Justine et al. However, the latter authors point out that the similarity of mature sperm is not sufficient to establish a phylogenic relationship between these taxa, since spermiogenesis may differ. Rohde, Watson & Roubal (1989a,b) and Rohde, Justine & Watson (1989) have subsequently shown that the flame bulb of Udonella differs fundamentally from that of all polyopisthocotylean and monopisthocotylean Monogenea examined and that Udonella cannot therefore be considered a monogenean. This shows that mature sperm can, apparently easily, acquire an identical ultrastructure by convergent evolution. Of great interest also is the finding that sperm structure of Polyopisthocotylea corresponds to the basic pattern of

996

K. ROHDE ANCYROCEPHALIDAE CALCEOSTOMATIOAE DACTYLDGYRIOAE DIPLECTANIDAE TETRAONCHIDAE

h4OtK03TYLIDAE

CAFSALIDAE

I8 d i! 8 2 5

GYROOACTYUDAE

WLYSTOMATIDAE HEXABOTHRIIDAE

DICLIDDPHORIDAE DISCOCOTYLIDAE GASTROCOTYLIDAE MAZOCRAEIDAE MICROCOTYLIDAE

FIG. 1I. Phylogeny of Monogenea based mainly on sensilla and ciliated patches according to Lambert (1980 a,b). Modified from Justine, Lambert & Mattei (1985).

0

/

ANCYROCEPHALIDAE CALCEOSTOMATTIDAE

MONOCOTYLIME LOIMOIDAE DIONCHIDAE CAPSALIOAE FUZETREMA LKJDNELLIME GYRCOACTYLIDAE

WLYSTOMATIOAE

\

HEXAGOTHRIIDAE HEXOSTOMATTIDAE PLECTANOCOTYLIDAE OICLIDOPl+3RIDAE GOTCCOTYLIDAE MICROCOTYLIOAE HETERAXINIDAE

\

EVOLUTIONARY TRENDS IN THE PLATYHELMINTHES

EUZETREMA

/

other Neodermata (two 9 + ‘1’ axonemes enclosed by a ring of microtubules), whereas the Monopisthocotylea have derived patterns. Hence, Polyopisthocotylea are more ‘primitive’, e.g. closer to the stem line than Monopisthocotylea, at least in this character, in contrast to the view of Mamaev & Lebedev (1979) who consider the former to be the ‘higher’ Monogenea.

5

& >

CEMOCOTYLIDAE

FIG. 12. Phylogeny of Monogenea based on sperm ultrastructure according to Justine, Lambert Jr Mattei (1985). Diagrams of cross-sections of mature sperm show axoneme(s) with central rod and complete, partial or lacking peripheral row of microtubules. Modified from Justine, Lambert & Mattei (1985).

Brooks (1989b) in his somewhat grandly named “unified theory of evolution”, postulated that evolutionary history is not just a passive accumulation of the effects of environmental selection over time (a view widely accepted and recently propagated by Price, 1980) but “driven by entropic accumulation of genetic information that is constrained and organized primarily by genealogical effects of phylogenetic history and developmental integration”, and only secondarily by ecological effects. Phylogenetic constraints are due to persistent ancestral traits that have not evolved rapidly enough to be affected by selection, and developmental constraints are due to the necessary integration of any new trait with the other traits to produce a viable organism. Genealogical (phylogenetic and developmental) processes are supposed to have “developmental, non-equilibrium, or diversifying effects”, whereas ecological processes tend to have homeostatic effects, “forcing populations into equilibrium conditions”. “The impact of phylogenetic and developmental constraints is to slow the natural entropic accumulation of genealogical events.” The predominant manifestations of the interaction between genealogical and ecological processes depend on the time scale, but on a macroevolutionary scale, with which we are concerned here, the ‘unified theory’ “predicts that the ecological and behavioural (functional) correlates of phylogeny should be conservative relative to the morphological and developmental correlates of phylogeny”. In other words, “closely related species will be morphologically distinct from but ecologically and behaviourally similar to each other and their common ancestor”. Also, ecological and behavioural traits should indicate the same phylogenetic relationships as structural data. Brooks (1989b) interprets his phylogenetic system of the Cercomeria as supporting the above predictions. However, as pointed out earlier, his system is largely based on traits whose homology has not been established, i.e. it is to a large degree phenetic. Such a phenetic approach leads to the false interpretation of convergence as phylogenetic relationship. Thus, the supposed relationship of dalyellioids (or other ‘turbellarian’ rhabdocoels) with the Neodermata is due to superficial similarities. If my system is correct, morphological convergence is responsible for the similarities between ‘turbellarian’ Rhabdocoela and Neodermata and within the genuinely related groups, morphological constancy is remarkable (identical

Phylogeny of Platyhelminthes protonephridia, sense receptors, neodermis, sperm in the Neodermata, etc.), contrary to the prediction made by Brooks. Ecological traits (as indicated, for example, by life-cycle patterns and hosts), on the other hand, differ extremely between groups such as between the various taxa of Digenea, between the Trematodes and Monogenea, etc., as recognized by Brooks but apparently not put in the proper perspective when comparing phylogenetic and ecological constraints. Malmberg (1974, 1982, 1986) posed the question as to whether evolution of the major parasitic platyhelminth classes was progressive or regressive. He (Malmberg, 1986) distinguished various “evolutionary capacity levels”. For example, he does not accept that the major platyhelminth classes have originated from a rhabdocoel-like ancestor (as often assumed), but believes that the ectolecithal egg and development used as evidence could merely indicate an origin from the same evolutionary capacity level. Furthermore, he suggests that already the very primitive placozoans, at the very base of the Metazoa, could represent “basically the first evolutionary level of hypothetical progenitors of the cercomeromorpheans and other platyhelminth groups”, and that an intestine has evolved more than twice in the platyhelminth line. If platyhelminths are arranged according to complexity, we get several progressive phylogenetic lines forming a ‘bush’ rather than a ‘tree’. In the Cercomeromorphae sensu Malmberg, i.e. the Cestoda, Amphilinidea, Gyrocotylidea and Monogenea, the first group is the most primitive and the last the most advanced. Nutriments were originally absorbed through the tegument and a digestive system has secondarily evolved only in the Monogenea. He concludes that, although the basic trend of evolution is progressive not only in the Cercomeromorphae but also in the Trematoda, there are also cases of regressive evolution in many parasitic platyhelminth groups, for example the loss of anchors and/or marginal hooks in certain Monogenea. Malmberg’s ideas, although interesting, contradict the results of cladistic analyses presented earlier, for instance by putting the Monogenea at the end and the Cestoda at the beginning of an evolutionary line. His concept of ‘evolutionary capacity level’ might still be valuable if used to indicate a similar complexity reached by two or more groups as a result of convergent or parallel evolution (e.g. by ‘turbellarian’ Rhabdocoela and Neodermata). If my system is accepted, a comparison of the most ‘primitive’ Neodermata, i.e the Aspidobothrea, with the other groups shows very clearly that aspidobothreans have by far the most complex nervous system and the greatest variety of sense receptors, both in the larva and the adult (Rohde, 1968,1970,1971a,b, 1972a,b, 1989a, in press; Rohde & Watson, 1989b, in press a,b,c). Complexity of nerves and receptors is also greater than known from any free-living flatworm taxon (for references see Rohde, 1989a). Among the cestodes, infective larvae of Austramphilina elongata

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(Amphilinidea) and Gyrocotyle urna (Gyrocotylidea) have an extraordinary variety of sense receptors (Rohde & Garlick 1985a,b,c; Rohde, Watson & Garlick, 1986; Xylander, 1987b), whereas larvae of the Cestoidea lack receptors (? or have at least a very strongly reduced receptor-nervous system). In the three phylogenetic systems discussed above, Cestoidea are placed at the very end of the phylogenetic line of cestodes and of all the parasitic Platyhelminthes. Our conclusion, then, must be that evolution to a parasitic way of life in the Platyhelminthes at first led to an enormous increase in the complexity of the nervousreceptor system; only later, in the ‘higher’ groups and presumably after a long adaptation to the hosts, has secondary simplification occurred. Kotikova (1986) also noted that transition to parasitism is accompanied by some progressive transformations in the nervous system of flatworms. Other authors have reached similar conclusions for smaller taxa of parasitic Platyhelminthes. Thus, Joffe (1981) concluded that, within the Temnocephalida, transition from free-living to commensal to parasitic way of life led to greater complexity, and Murith (1981) concluded that in the Polystomatidae (Monogenea), the group with ancestral species has the most complex chaetotaxy (pattern of sensilla). Mamkaev (1986) found that the evolutionarily primitive groups show the greatest variety of morphofunctional systems and morphogenetic mechanisms. He even considers this correlation a “criterion of evolutionary primitiveness”. According to him, examples are the Turbellaria as a whole, which are more diverse that other groups of Scolecida (worms of the ‘lower’ phyla), and among the Turbellaria, the Acoela. Evidence on the ultrastructure of protonephridia in the Platyhelminthes supports Mamkaev’s conclusion: the terminal taxa of the two phylogenetic lines recognized by me, i.e. the Neodetmata and ‘turbellarian’ Rhabdocoela, each have a type of flame bulb with little variation (the one major difference is that between trematodes/monogeneans and cestodes), whereas a considerable variability is found in the more ‘primitive’ Macrostomida. Among the Neodermata, the ‘primitive’ aspidobothreans show the greatest variety of sense receptors, and even among species in one family, the Aspidogastridae, Rohde (in press) noticed marked differences in the ultrastructure of receptors of three species. Since the host ranges of aspidobothreans are known to be wide, it is unlikely that divergence of receptors is an adaptation to a specific host. It is more likely that such divergence is due to the archaic nature, i.e. the long history, of the group (Rohde, in press). The variety of receptor types in adult Aspidobothrea contrasts sharply with the relative uniformity of receptors in adult Digenea and other ‘higher’ Neodermata. Cestoidea, at the end of the phylogenetic line, seem to have the smallest variety of receptors. However, it must be pointed out that greater diversity of more archaic taxa seems to be restricted to characteristics of

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K. ROHDE

the basic body plan, and ‘higher’ forms, such as Digenea and Cestoidea have a very great variety of life-cycle patterns, as well as of types of cercariae and scolices, respectively, etc. AN ALTERNATIVE

HYPOTHESIS:

MOSAIC

EVOLUTION? Standard evolutionary theory (like the discussion so far) assumes that, at least in higher eukaryotes, organisms evolve as a whole. Phylogenetic systematics (cladistics) assumes the same and explains similarities in different phylogenetic lineages by convergent evolution. However, recent studies have shown that in prokaryotic organisms horizontal gene transfer between species is common, with evolutionary consequences. Gene transfer is also known from lower eukaryotes (Lang, 1984; Waring, Brown, Ray, Scazzocchio & Davies, 1984), for which retroviruses may be responsible (Benviste & Todaro, 1974; Gruskin, Smith & Goodman, 1987). Host plants and symbiotic bacteria can exchange genes (Drummond, 1979; Carlson & Chelim, 1986). Lavitrano, Camaioni, Fazio, Dolci, Farace & Spadafora (1989) have claimed that, under experimental conditions, transgenic mice can be obtained using sperm cells as foreign DNA vectors (by mixing washed sperm with cloned DNA and using the sperm to fertilize mouse eggs which are then placed into the oviducts of foster mothers). Birnstiel & Busslinger (1989) have pointed out that the last findings need verification and that, even if replicated, gene transfer “would lead in the main to only a transitory appearance of foreign DNA” since “most eukaryotic sequences, when transferred, are likely to be selectively neutral, and will have a low probability of becoming fixed throughout the population” (for a discussion of horizontal gene transfer see Syvanen, 1987). Howell (1985) proceeding from the established fact that some parasites at least have the genetic capacity to synthesize macromolecules either identical or closely resembling those of their hosts, assumed that the parasites’ genomes contain DNA sequences identical or similar to those of their hosts. General explanations for this phenomenon are that such homology represents either conservation over very long periods or recent adaptive change, but Howell argues that it may have arisen by “direct incorporation of host genetic material into the parasite genome”, possibly by retroviruses. He suggests that the following evidence for gene exchange between host and parasite should be looked for: (1) the existence of retroviruses common to both hosts and parasites; (2) DNA sequence homologies between host, parasite and virus genomes (for example by the Southern blotting technique). Studies of symbiotic associations have yielded more and more evidence that “the functional boundaries of organisms may not be exclusive or discrete”; “the image of the genome as a stable entity, replicating faithfully generation after generation, is less and less

well-supported”, and “there may be strong selection pressures for organisms in symbiotic associations to exchange genes and to maintain those genes that have been acquired” (Dyer, 1989) (see also the brief review by Maynard Smith, 1989). Concerning the very base of cellular organisms, the cell itself, it is widely accepted now that evolution of the eukaryotic cell was due to the symbiosis of several more primitive organisms (Margulis, 1970, 1981). For details of the various hypotheses of the origin of eukaryotes see, for instance, Ahmadjian & Paracer (1986) and for a general discussion of ‘symbiogenesis’ as a macromechanism of evolution see Schwemmler (1989). In summary, the evolutionary significance of gene transfer even among higher eukaryotes, to which the Platyhelminthes belong, must be considered a possibility, although definitive evidence is not yet available (for probable cases see Syvanen, 1987). Even if a successful transfer of evolutionary significance should occur only rarely, it may still have a profound impact on the phylogeny of many groups. If a transfer would be major, perhaps leading to drastic reorganization of a trait, it could result in morphologicaldevelopmental-behavioural, etc. similarities between two lineages usually explained by convergent evolution, i.e. evolution of similarities resulting from strong selective pressure. Organisms, then, would not evolve as a whole, but-to a certain degree-the units of evolution would be character traits, exchangeable between phylogenetic lines and resulting in a process which might be called mosaic evolution. Phylogenetic systematics, which is based on the assumption of organisms as the units of evolution, would have to be abandoned as a method to determine phylogenetic relationships between organisms. It could become, in a modified form, a method to determine relationships between traits. A decision as to whether convergent or mosaic evolution explains similarities between groups, can be made on the basis of the following evidence: (1) direct evidence of gene transfer (for example using DNA/ RNA sequencing); (2) occurrence of identical or very similar homologous character traits (including DNA/ RNA sequences) in two unrelated groups, i.e. in groups which have a great number of different traits likely to be homologous within each group; (3) frequent appearance of seemingly ‘convergent’ traits in several lineages which have been exposed to different selection pressures and are therefore unlikely to have many truly convergent characters. Mosaic evolution might explain the conflicting evidence for the relationships of many taxa. SUGGESTIONS FOR FURTHER RESEARCH Major advances in our understanding of flatworm phylogeny can be expected from 18SrRNA studies which are now underway. However, it would be a mistake to expect that such studies would make morphological and developmental studies superflu-

Phylogeny

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of Platyhelminthes

ous. As pointed out above, different molecular methods do not always give consistent results. More ‘classical’ methods are necessary to validate molecular results and consistency must be demonstrated between the two approaches (in cases where phylogenetic relationships have been established beyond doubt by morphological/developmental studies). Furthermore, we are obviously not only interested in proving a relationship between X and Y, but also in the characteristics of X and Y. Thus, combined molecular, morphological and developmental studies can provide deeper insights into the evolutionary mechanisms in particular groups. Concerning morphological and particularly ultrastructural approaches, we know that comparative studies of sperm and spermatogenesis have made useful contributions to understanding the phylogeny of platyhelminth taxa at various levels (e.g. Franz&, 1970; Hendelberg, 1970, 1974, 1977a,b, 1983a,b, 1986; Rohde, 1971a; Tuzet & Ktari, 1971a,b; Tyler & Rieger, 1975; Halton & Hardcastle, 1976; Kritsky, 1976; Rees, 1979; Euzet, Swiderski & MokhtarMaamouri, 1981; Jamieson & Daddow, 1982; Justine & Mattei, 1981, 1982a,b, 1983a,b,c,d, 1984a,b,c,d, 1985a,b,c,d, 1986, 1987; Justine, 1982, 1983, 1986; Afzelius, 1983; Mohandas, 1983; Williams, 1984; Justine, LeBrun & Mattei, 1985a,b; Sopott-Ehlers & Ehlers, 1986; Cifran, Garcia-Corrales & Martinez Al&, 1988; Rohde & Watson, 1986; Noury-Srai’ri, Justine & Euzet, 1989a,b; Sopott-Ehlers, 1989; for phylogenetic significance of sperm studies in Metazoa in general see Wirth, 1984). Additional studies are important to clarify the phylogenetic position of many taxa. In particular, detailed studies of the 9 + 1 axoneme pattern of sperm of several species of Acoela and of spermiogenesis in Macrostomida are necessary to demonstrate or exclude a relationship with the Trepaxonemata. Among the Neodermata, spermiogenesis of Udonella needs examination to clarify how the similarity of the mature sperm with that of Monogenea is brought about. Recent findings on the occurrence of centriolar plates in spermiogenesis indicate that such plates may be characteristic of certain taxa and therefore useful for phylogenetic studies (Rohde & Watson, 1986; Sopott-Ehlers, 1989). Particular ultrastructure of epidermal locomotory cilia including their rootlets is known to be characteristic for certain taxa (e.g. Tyler, 1979; Hendelberg, 1981; Rohde, 1986b, Rohde, Watson & Cannon, 1988c), and more extensive studies of additional taxa are necessary. Briiggemann (1986a) and Martens (1986) have examined the ultrastructure of genital hard structures in Turbellaria and similar comparative studies of free-living and parasitic forms may contribute to our understanding of their phylogeny. The ultrastructure of the flame bulbs of many species of free-living and parasitic Platyhelminthes has been studied (references in Ehlers, 1985a; Rohde, 1986a, 1989b; Ruppert & Smith, 1988; recent papers

by Ehlers & Sopott-Ehlers, 1987; Kunert, 1988; Ehlers, 1989; Rohde, Watson & Roubal, 1989a,b; Rohde, Noury-Srdiri, Watson, Justine & Euzet, in press; Rohde, Watson & Sluys, in press). However, many taxa have not yet been examined and several species of each large taxon (family, order, class) should be examined for information about variability of these structures. Only a single ultrastructural study of the development of flame bulbs has been made, that by Rohde & Watson (1988a) on the amphilinid Austramphilina. Similar studies of trematodes and monogeneans are necessary to show whether the presence of a junction in flame bulbs and capillaries in these groups indicates a fundamentally different formation of the terminal parts of the protonephridia. Similar studies of tubellarians may help in tracing a sister group of the Neodermata, and in establishing relationships between the various turbellarian taxa. As pointed out above, the ultrastructure of pharynges in Platyhelminthes is practically unknown, and studies of the pharynx of various groups are necessary. Coomans (198 1), von Salvini-Plawen (1982), Vanfleteren (1982) and Fournier (1984), among others, have discussed phylogenetic implications of photoreceptor structure, and examination of the ultrastructure of photoreceptors of larval Neodermata and Turbellaria may indicate phylogenetic relationships. Presumptive mechano- and/or chemoreceptors of Neodermata are characterized by electron-dense collars (e.g. Ehlers, 1985a), and an extensive search among the Turbellaria may reveal collars more similar to the neodermatan ones than hitherto known. Other studies potentially useful for phylogenetic conclusions include those of the ultrastructure of vitellaria (e.g. Xylander, 1987a), epidermis and tegument (reviews by Bedini & Papi, 1974; Tyler, 1984), gross morphology and histochemistry of nervous systems (e.g. Kotikova, 1986; Kotikova & Joffe, 1988; Joffe & Kotikova, 1989), ultrastructure of secretory granules (Noury-Srai’ri, Justine & Euzet, 1990) and rhabdites (e.g. Smith, Tyler, Thomas & Rieger, 1982), function of hooks in ‘cercomer’ (Rohde & Watson, 1989a), and embryology (e.g. Thomas, 1986). Urgently needed are life-cycle studies of Gyrocotyle and of aspidobothreans of uncertain status (Rugogaster, Stichocotyle, etc.) Acknowledgements-Financial support for the studies on which much of this review is based was given by the Australian Research Council and the University New England. Mv special thanks are due to Dr N. Watson for her tireless help with the electron microscope studies and for critically reading the manuscript. M. Notestine and S. Higgins typed the manuscript.

of

REFERENCES AFZELIUS B.

1983. Sperm ultrastructure in relation and phylogeny. In: The Sperm Cell (Edited ANDRE J.), pp. 385-394. Martinus Nijhoff, The Hague.

function

to by

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