Systematic Parasitology 26: 1-32, 1993. 1 © 1993 Kluwer Academic Publishers. Printed in the Netherlands.

Phylogeny and a revised classification of the Monogenoidea Bychowsky, 1937 (Platyheiminthes)

Walter A. Boeger ~ and Delane C. Kritsky 2 ~Departamento de Zoologia, Universidade Federal do Parand, Caixa Postal 19020, 81531, Curitiba, Parand: and Conselho Nacional de Desenvolvimento Cientifico e Tecnol6gico, Brasil 2College of Health-Related Professions, Box 8090, Idaho State University, Pocatello, ID 83209, USA

Accepted for publication 5th August, 1992

Abstract

A hypothesis (CI = 57.3%) on the evolutionary relationships of families comprising the class Monogen- oidea is proposed based on 141 character states in 47 homologous series and employing phylogenetic systematics. Based on the analysis, three subclasses, the Polyonchoinea, Polystomatoinea and Oligoncho- inca, are recognised. The analysis supports independent origins of the Montchadskyellidae within the Polyonchoinea and of the Neodactylodiscidae and Amphibdellatidae within the order Dactylogyridea (Polyonchoinea); the suborder Montchadskyellinea is raised to ordinal status and new suborders Neodac- tylodiscinea and Amphibdellatinea are proposed to reflect these origins. The Gyrodactylidea (Polyoncho- inca) is supported by three synapomorphies and comprises the Gyrodactylidae, Anoplodiscidae, Tetraon- choididae and Bothitrematidae. The analysis supports recognition of the Polystomatoinea comprising Polystomatidae and Sphyranuridae. Evolutionary relationships within the Oligonchoinea indicate indepen- dent origins of three ordinal taxa, the Chimaericolidea (monotypic), Diclybothriidea (including Di- clybothriidae and Hexabothriidae) and Mazocraeidea (with five suborders). The suborder Mazocraeinea comprises the Plectanocotylidae, Mazocraeidae and Mazoplectidae, and is characterised by two synapo- morphies. The suborder Gastrocotylinea, characterised by presence of accessory sclerites in the haptoral sucker, is divided into two infraorders, the monotypic Anthocotylina infraorder novum and Gastrocotyl- ina. Two superfamilies of the Gastrocotylina are recognised, the Protomicrocotyloidea and Gastrocotyl- oidea; the Pseudodiclidophoridae is considered incertae sedis within the Gastrocotylina. The suborder Discocotylinea comprises the Discocotylidae, Octomacridae and Diplozoidae and is supported by four synapomorphies. The monotypic Hexostomatinea suborder novum is proposed to reflect an independent origin of the Hexostomatidae within the Mazocraeidea. The terminal suborder Microcotylinea comprises four superfamilies, the Microcotyloidea, Allopyragraphoroidea, Diclidophoroidea and Pyragraphoroidea. The analysis supports incorporation of the Pterinotrematidae in the Pyragraphoroidea and rejection of the monotypic order Pterinotrematidea. The following taxa are also rejected for reasons of paraphyly and/or polyphyly: Articulonchoinea, Bothriocotylea, Eucotylea, Monoaxonematidea, Tetraonchidea, Go- tocotyloidea, Anchorophoridae and Macrovalvitrematidae. The Sundanonchidae, Iagotrematidae and Microbothriidae were not included in the analysis because of lack of pertinent information regarding character states.

2 W.A. Boeger and D.C. Kritsky

Introduction

The phylogenetic relationships of the Monogeno- idea* have been controversial since Bychowsky (1937, 1957) revived Spengel's (1905) notion of consanguinity of the cestodes and monogenoide- ans. Bychowsky's phylogenetic hypothesis and classification for the Monogenoidea, based pri- marily on larval characters, differed from the then contemporary and established system of Fuhrmann (1928), who promoted sister relation- ship of the digeneans and monogeneans as pro- posed by Janicki (1921). Bychowsky's system has been frequently revised to accommodate new dis- coveries (e.g. Gusev, 1976, 1977, 1978a,b; Le- bedev, 1987, 1988, 1989; Mamaev & Lebedev, 1977, 1979); subsequent efforts at classification by Price (1936, 1937a,b, 1938a,b, 1939a,b, 1942, 1943a,b, 1961a,b, 1962a,b), Sproston (1946) and Yamaguti (1963) represent expansion and/or modification of Fuhrmann's ideas. Llewellyn (1963, 1965, 1970) outlined a phylogenetic hypo- thesis for the Monogenoidea utilising larval and some post-larval features primarily of the haptor. LleweUyn did not provide a congruent classifica- tion, but his analysis suggested additional evolu- tionary avenues within the class. Malmberg (1990) proposed a classification based on haptoral struc- tures and on the premise that evolution is pro- gressive, i.e. structures are added as evolution proceeds. Apparently an outcome of his evolu- tionary premise, Malmberg's system deviates most significantly from the other published proposals for the Monogenoidea. Finally, Justine's (1991) phylogenetic hypothesis and classification for some groups of Monogenoidea was based on ul- trastructural information on sperm and spermiog- enesis.

A common "thread" among the work outlined above is that each is based on a single or a few sets of characters, while ignoring other potentially useful homologies within the group. In the present study, the monogenoidean families are subjected

* Use of the appelation 'Monogenoidea ' rather than the more commonly used 'Monogenea ' is at the insistence of the authors. It does not reflect editorial policy or approval. Ed.

to cladistic methods in order to examine their evolutionary relationships based on a variety of anatomical and ultrastructural characters. A re- vised classification of the class grounded on the new phylogenetic hypothesis is provided.

Materials and methods

Character states for each familial taxon were in- itially defined from the literature. Published ac- counts were verified, when possible, by subse- quent examination of representative specimens of each monogenoidean family from museum and private collections (see Addendum II). However, some potentially useful transformation series were not included in the analysis due to lack of infor- mation on character states for most families. Homologous series in which the apomorphic state is an autapomorphy of a single family generally were not utilised in the reconstruction of the phy- logeny.

An initial hypothesis on evolutionary relation- ships of the families of Monogenoidea was con- structed using Hennigian Argumentation (Hen- nig, 1966; Wiley, 1981); the topology of the cladogram was then subjected to PAUP (Phylo- genetic Analysis Using Parsimony, Version 2.4.1; D. L. Swofford, Illinois Natural History Survey, Champaign) to confirm that it was a most-parsi- monious tree. A total of 141 character states com- prising 47 transformation series was used in the analysis. Polarisation of homologous series was determined by outgroup analysis and optimised according to procedures described by Watrous & Wheeler (1981) and Maddison et al. (1984). Func- tional outgroups were used when character states of a transformation series were entirely within the ingroup (Watrous & Wheeler, 1981). The Udonel- lidea, Trematoda, Gyrocotylidea and Cestoidea were chosen is outgroups based on the phylogen- etic reconstruction of the Cercomeria by Brooks et al. (1985) and Brooks (1989a,b). In our revised classification of the Monogenoidea, the principles of "priority" and "coordination" set forth in re- spective Articles 23 and 36 of the 1985 Interna- tional Code of Zoological Nomenclature (ICZN)

Phylogeny and classification of the Monogenoidea 3

were utilised for determination of taxonomic names and their authorship. Configuration of taxa, based on included subordinate taxa, was not used as criteria for proposal of new taxa above the family level; available names with priority at the class and ordinal levels were used whenever possible. As a result, we use the name Monogeno- idea Bychowsky, 1937, since it was the first pro- posed for the group at the rank of class (see 'Dis- cussion' and Lebedev, 1988).

Results

Character analysis

Homologous series utilized in the analysis follow with comments on character evolution. Numbers in parentheses preceding a character state refer to the coding that state received in the data matrix; bold numbers in brackets following the definition of a character state refer to respective evolution- ary changes depicted in the cladogram. A list of character state changes with homoplasies is pro- vided in Addendum I; the data matrix is available on computer disc through the University of Neb- raska State Museum, Lincoln, Nebraska (HWML 35503).

1. Eyes in oncomiracidium. Plesiomorphy: (000) two pairs [5, 155]. Apomorphies: (010) two pairs, posterior pair fused [71]; (100) one pair fused [115]; (200) two pairs, anterior pair fused [159]; (991) eyes absent [24, 49, 66, 85, 96, 110, 167]. Transformation of this series is presented in Fig. 1 (coded by mixed coding = nonredundant linear coding, see O'Grady & Deets, 1987). 2. Eyes in adult (when present in oncomiracid- ium). Plesiomorphy: (00) two pairs [6]. Apo- morphies: (01) two pairs, posterior pair fused [54]; (10) eyes absent [116]. Derived states evolved in- dependently (coded by additive binary coding, see O'Grady & Deets, 1987). Families for which the state of the oncomiracidium is not known and the adult lacks eyes were coded (99) since it could not be determined if the eyes in the adult were absent

(010) "~/'~

(091) xx x

(000) [ .

~ (200) (lOO)

Fig. 1. Hypothesised transformation of character states of the eyes in the oncomiracidium (diagrammatic). Broken arrows represent potential transformations not thought to have oc- curred in the evolution of family taxa in the Monogenoidea. Numbers in parentheses indicate the respective code each state received in the matrix (homologous series 1).

because of evolutionary loss or ontogenetic con- straint. 3. Position of mouth. Plesiomorphy: (0) subtermi- hal [35]. Apomorphy: (1) ventral [7, 103]. 4. Oral suckers. Plesiomorphy: (00) circumoral sucker present. Apomorphies: (10) oral sucker absent [19, 104]; (01) two oral suckers (buccal organs) present [111]. Apomorphies evolved inde- pendently (coded by additive binary coding). 5. Gut. Plesiomorphy: (0) double. Apomorphy: (1) single [50, 69, 150]. The analysis supports polarisation proposed by Brooks (1989b). The sin- gle gut in the Diplozoidae may represent a derived "double" gut, in which the oesophagus extends the major length of the body to the level of the germarium where bifurcation occurs; one caecal branch is significantly reduced (or absent) while the other extends into the haptor with or without diverticula (see fig. 2 in Khotenovsky, 1985). If the diplozoid gut is a specially derived bifurcated gut, no homoplasy in this series would occur be- tween the Polyonchoinea and Oligonchoinea. 6. Caeca. Plesiomorphy: (0) nonconfluent. Apo- morphy: (1) confluent [25, 83]. Initially we con- sidered confluence of simple caeca as the same

4 W.A. Boeger and D.C. Kritsky

state as anastomoses of intestinal diverticula. Early phylogenetic analyses indicated that anas- tomoses of diverticula and confluent intestinal caeca correspond to independent evolutionary events. Thus, the character states in this transfor- mation series apply only to taxa primitively lack- ing gut diverticula. Taxa with diverticula (see character 7) receive a (9) in the matrix as do those in which the gut is single (see character 5) or information on the gut is wanting.

The Dactylogyridae and Pseudomurraytremati- dae contain species with both confluent and non- confluent caeca. In these families, the analysis suggests that nonconfluence is primitive and that confluence developed independently within clades of the respective families. 7. Gut diverticula. Plesiomorphy: (0) absent. Apomorphy: (1) present [36, 51, 91]. Some po- lyonchoinean and polystomatoinean families with the plesiomorphic state have species with gut di- verticula. The development of diverticula in these families (e.g. Capasalidae, Monocotylidae, Polys- tomatidae) apparently represents secondary evolutionary phenomena. 8. Testes. Plesiomorphy: (00) single [148]. Apo- morphies: (10) double [26]; (01) more than two [76]. Apomorphic states evolved independently from the plesiomorphic state (coded by additive binary coding). 9. Position of testis(es). Plesiomorphy: (0) pos- terior to germarium. Apomorphy: (1) anterior to germarium [128]. 10. Vas deferens. Plesiomorphy: (0) intercaecal. Apomorphy: (1) looping left caecum [33]. 11. Sperm axonemes. Plesiomorphy: (00) two ax- onemes. Apomorphies: (10) two axonemes (one reduced) [14]; (91) one axoneme [55, 57]. 12. Sperm microtubules. Plesiomorphy: (00) lying along entire cell periphery. Apomorphies: (10) lying along 1/4 of cell periphery [8]; (01) absent [20]. 13. Male Copulatory organ. Plesiomorphy: (0) muscular [27, 46]. Apomorphy: (1) sclerotised [9]. Brooks et al. (1985) and Brooks (1989b) postu- lated that the plesiomorphic state for monogeno- ideans is presence of a sclerotised copulatory organ and consider it homologous to the "cop-

ulatory stylet" of dalyelloids, udonellids and tem- nocephalids. Comparative morphology of the stylet of dalyelloids does not support this hom- ology. Further, udonellids do not possess a scler- otised copulatory organ; Brooks and co-workers apparently considered the Anoplodiscidae (herein included in the Gyrodactylidea) a member of the Udonellidea after Palombi (1943 - in Yamaguti, 1963) which may explain their polarisation. Al- though the state in some temnocephalids is similar to that of most polyonchoineans, optimization of the transformation series (including states in tem- nocephalids, dalyelloids and udonellids) supports the present polarisation.

Another potentially useful feature for phylo- genetic analysis of the Monogenoidea is expressed in the mode by which the male copulatory organ functions during copulation, i.e. protrusion or eversion. Although this functional feature may already be expressed to some extent in our analy- sis by the morphological characters we use, a hom- ologous series including "mode of action of the male copulatory organ" was not included because of insufficient information concerning the action of the male copulatory organ in members of many familial taxa. 14. Accessory piece. Plesiomorphy: (0) absent. Apomorphy: (1) present [34]. 15. Muscular male copulatory organ. Plesiomor- phy: (0) ovate. Apomorphy: (1) elongate [10, 105, 131, 140, 174]. 16. Spines of male copulatory organ (copulatory organ muscular). Plesiomorphy: (0) present. Apo- morphy: (1) absent [11, 133, 143, 154]. 17. Sac of male copulatory organ (copulatory organ muscular). Plesiomorphy: (0) absent [130, 142]. Apomorphy: (1) present [28, 106, 125, 172]. 18. Genital aperture (when single). Plesiomorphy: (0) lying on mid-line. Apomorphy: (1) marginal [21, 134]. The surface pores of the male and fe- male reproductive systems in members of the Gyrodactylidae are widely separated (Kritsky, 1970; Kritsky & Boeger, 1991). In diplozoids, two adults are fused in permanent copula, and the male system does not communicate with the body surface, although uterine pores are present in each individual of the diplozoan pair (see Khotenov-

Phylogeny and classification of the Monogenoidea 5

sky, 1985). The Gyrodactylidae and Diplozoidae receive a (9) in the matrix; respective states are autapomorphies that do not contribute evolution- ary information regarding the ingroup. 19. Genital atrium. Plesiomorphy: (0) unarmed. Apomorphy: (1) armed [158, 175]. 20. Bilateral, armed muscular pads of genital at- rium. Plesiomorphy: (0) absent [162]. Apomor- phy: (1) present [157]. 21. Germarium. Plesiomorphy: (00) ovate. Apo- morphies. (01) lobate [95]; (10) elongate, U- shaped [99, 122]; (20) elongate, inverted U- shaped [112]; (30) elongate, double inverted U- shaped [156]. See Fig. 2 for ordering (coded by mixed coding). 22. Pathway of germarium/oviduct. Plesio- morphy: (0) intercaecal [74]. Apomorphy: (1) looping right caecum [17, 37, 60]. Our analysis indicates that the looping of the germarium/ovid- uct around the right caecum represents conver- gent states in several clades in the Polyonchoinea. The germarial loop is plesiomorphic for the four terminal suborders of the Dactylogyridea (Dactylogyrinea, Tetraonchinea, Amphibdellati- nea, Neodactylodiscinea) supporting the polaris- ation offered by Kritsky & Boeger (1989) for the Dactylogyridae. 23. Genito-intestinal canal. Plesiomorphy: (0) ab- sent (Fig. 3A). Apomorphy: (1) present (Fig. 3B) [77]. Bychowsky (1957) states, "the homology of the canalis genito-intestinalis of Monogenoidea and Turbellaria cannot be subjected to any doubt". However, outgroup comparison suggests that absence of the genito-intestinal canal is plesi- omorphic for the Monogenoidea, but reversal of the polarisation of this homologous series does not affect either the topology nor the consistency of the final cladogram. 24. Vagina. Plesiomorphy: (000000) one ventrola- teral "true" vagina. Apomorphies: (010000) one midventral "true" vagina [32, 39]; (000100) two lateral "true" vaginae [64]; (100000) two lateral "ductus vaginalis" [81]; (200000) one mid-dorsal "ductus vaginalis" [138, 153]; (300000) two dorsal "ductus vaginalis" [141, 161]; (100010) one ven- tro-lateral "ductus vaginalis" [129]; (101010) one mid-ventral "ductus vaginalis" [136]; (000001) va-

gina absent [48]. See Fig. 4 for transformation of the states in this series (coded by mixed coding); see Fig. 3 for configuration of female reproductive system with "true" vagina (Fig. 3A) and with "ductus vaginalis" (Fig. 3B).

The presence of bilateral vaginae ("ductus vagi- nalis") was considered plesiomorphic for the Monogenoidea by Brooks et al. (1985). However, a single lateral vagina ("true" vagina) is present in outgroups as Laurer's canal in the Digenea (see Bychowsky, 1957) and as the vagina of Cestoidea. Optimisation indicates that the state, single ven- tro-lateral "true" vagina, is plesiomorphic for the ingroup. 25. Egg. Plesiomorphy: (0) oval [47, 67]. Apo- morphy: (1) tetrahedral [18, 29, 40]. 26. Egg filaments. Plesiomorphy: (00) one fila- ment [151, 169]. Apomorphies: (10) two filaments [113]; (91) filaments absent [82, 107, 147]. The series is coded by additive binary coding. Loss of structures usually does not leave morphological "clues" concerning origin of the state. By coding the absence of egg filaments as (91) we recognise that loss may have resulted from either single or double filamented eggs. 27. Shape of haptor. Plesiomorphy: (0) disc shaped. Apomorphy: (1) dactylogyrid [62]. 28. Number and distribution of ("domus bear- ing") hooks in oncomiracidium. Plesiomorphy: (000) 16 marginal (Fig. 5A) [1, 43]. Apornorphies: (991) 14 marginal (Fig. 5B) [15, 30, 93]; (100) 14 marginal, 2 central (Fig. 5C) [12]; (200) 12 marginal, 2 central (Fig. 5D) [58, 72]; (010) 10 marginal (Fig. 5E) [100]; (020) 6 marginal (Fig. 5F) [145]; (030) 4 marginal (Fig. 56) [149]. The transformation of these states is presented in Fig. 5 and coded by additive binary coding. Polaris- ation suggested by outgroup comparison (plesi- omorphy = 10 marginal hooks) was initially con- sidered but rejected by parsimony.

The cladogram suggests many instances where "16 hooks" evolved into "14 hooks". However, the occurrence of 14 hooks is not necessarily a result of homplasious events. Haptors with 14 hooks might have evolved from a 16-hook state via at least 8 different nonconvergent ways, i.e. there are 8 pairs of hooks, each with potentially

6 W.A. Boeger and D.C. Kritsky

(oo) (Ol)

2 Fig. 2. Proposed transformation of types of germaria in the Monogenoidea (diagrammatic). Numbers in parentheses indicate the respective code each state received in the matrix (homologous series 21).

equal probability of being lost. Consequently, the 14 hook states of the Calceostomatidae and Dac- tylogyridae (12 marginal, 2 central) are not hom- ologous to states exhibited by the Monocotylidea and Dionchidae (14 marginal). The analysis also indicates that those of the latter two taxa are a result of independent loss of the central hook pair, and that the"12 marginal, 2 central" states of the Dactylogyridae (plus its sister taxa) and the Cal- ceostomatidae are derived from independent loss of one marginal pair. We coded the state "14 marginal hooks" as (991) to avoid subjective de-

termination of the ancestral condition for this state. 29. Number and distribution of ("domus bear- ing") hooks in adult. Plesiomorphy: (00000) 16 marginal (Fig. 6A) [2, 44]. Apomorphies: (99199) 14 marginal (Fig. 6B) [16, 31, 38, 94]; (10000) 14 marginal, 2 central (Fig. 6C) [13]; (10001) 12 marginal, 2 central (Fig. 6D) [59]; (20000) 10 mar- ginal, 2 central, 4 dorsal (Fig. 6F) [61]; (30000) 8 marginal, 2 central, 4 dorsal (Fig. 61) [73]; (01000) 2 ventral (Fig. 6E) [97]; (02000) 2 ventral, 4 in each of two lappets (Fig. 6G) [170]; (99919) hooks

Phylogeny and classification of the Monogenoidea 7

.dv

,0

A

, I i

g

//-OV 0

B 3 Fig. 3. Basic types of female reproductive systems in the Monogenoidea (diagrammatic): A, vagina connecting to oviduct ("true" vagina), genito-intestinal canal absent; B, vagina connecting to vitelline ducts ("ductus vaginalis"), genito-intestinal canal present. Abbreviations: dv, "ductus vaginalis"; g, gut; gi, genito-intestinal canal; o, germarium; oo, o6type; ov, oviduct: u, uterus; v, "true" vagina; vc, vitelline canal.

absent (Fig. 6H) [52, 108]. The transformation for the states of this series is presented in Fig. 6 (coded by mixed coding). The states "hooks ab- sent" and "14 marginal hooks" were appro- priately coded to avoid subjective assignment of ancestral states (see comments on series 28). Polarisation by outgroup comparison suggests that the plesiomorphic state for this series is hooks absent; however, this state is rejected as primitive by parsimony. 30. Shape of hooks. Plesiomorphy: (0) unhinged (Fig. 7A). Apomorphy: (1) hinged (Fig. 7B) [22, 45]. Gerasev (1987) and Malmberg (1990) suggest homology of the acanthocotylid hook and the gyr- odactylid hook based on presence of a "hinge" between the hooklet and shank. The present analysis indicates that the hinged articulation de- veloped independently in these groups.

31. Anchor. Plesiomorphy: (0) present in at least one stage of development [3]. Apomorphy: (1) absent in all stages of development [23, 53, 146, 166]. Absence of anchors was initially considered plesiomorphic. However, the analysis indicates that the ancestor of the Monogenoidea possessed one pair of anchors in the adult stage. Conse- quently, there have been many instances of loss of anchors during evolution of the class. 32. Number of anchors (when present in at least one developmental stage). Plesiomorphy: (0) one pair, ventral [4]. Apomorphies: (1) two pairs, ven- tral [56]; (2) two pairs, one ventral, one dorsal [65]. Polarisation is by functional outgroup com- parison. 33. Bars (when anchors present in at least one developmental stage). Plesiomorphy: (00) absent [63]. Apomorphies: (10) one ventral [41]; (11) two

8 W.A. Boeger and D.C. Kritsky

ONE MIDVENTRAL "TRUE" VAGINA (010000)

TWO LATERAL "TRUE" VAGINAE

~ 0100) VAGINA ABSENT (00007

ONE VENTROLATERAL "TRUE" VAGINA (oooooo)

1 TWO LATERAL "DUCTUS VAGINALIS" (100000)

ONE VENTROLATERAL "DUCTUS VAGINALIS" ONE MIDDORSAL "DUCTUS VAGINALIS" (100010) (200000) l

ONE MIDVENTRAL "DUCTUS VAGINALIS" TWO DORSAL "DUCTUS VAGINALIS" ,10,010, , 00000, 4

Fig. 4. Postulated transformation of states of vaginae in the Monogenoidea. Numbers in parentheses indicate the respective code each state received in the matrix (homologous series 24).

ventral [42]; (20) one ventral, one dorsal [68]; (30) one ventral, two dorsal [70, 75]. 34.Haptoral suckers in adult. Plesiomorphy: (0) absent. Apomorphy: (1) present [78]. The haptor- al suckers of most (but not all) of the Mazocraei- dea function in various ways as a clamp. As a result, the term "clamp" has been in general use for these structures in mazocraeidean species. In the present analysis, however, we use "haptoral sucker" to connote the proposed homology of the suckers lacking sclerites of the Polystomatoinea and those with sclerites of the Diclybothriidea, Chimaericolidea and Mazocraeidea. 35. Haptoral suckers in oncomiracidium. Plesi- omorphy: (0) absent. Apomorphy: (1) present [144]. The series is polarised by functional out- group comparison. 36. Fire-tong sucker (haptoral suckers present). Plesiomorphy: (0) absent. Apomorphy: (1) pre- sent (Fig. 8L,M) [168]. Polarisation is by func- tional outgroup comparison. 37. Association of hook and haptoral sucker (hap- toral suckers present). Plesiomorphy: (0) present in adult [79]. Apomorphy: (1) present during de- velopment but absent in adult [98]. Polarisation of the series is by functional outgroup comparison. 38. Number of haptoral suckers (suckers present). Plesiomorphy: (00000) three pairs [80]. Apo-

morphies: (01000) one pair [84]; (10000) four pairs [90]; (20000) numerous pairs, microcotylid [160]; (10100) numerous pairs, gastrocotylid [135, 137]; (10010) numerous pairs, diclidophorid [164]; (10001) numerous pairs, fire-tong (Fig. 8L,M) [173]. The proposed transformatton is presented in Fig. 9 (coded by mixed coding). Three states (one, three, and four pairs of haptoral suckers) are equally parsimonious as the synapomorphy for the clade Polystomatoinea + Oligonchoinea.

Initially, the states involving "multiple" hapto- ral suckers were considered a single state. Result- ing hypotheses suggested many unlikely instances within the Mazocraeidea were multiple pairs of suckers reversed to the more primitive, "four pairs", without regard for sucker type. Thus, the coding of states in this series incorporates infor- mation on sucker type and number. 39. Haptoral suckers in appendix (suckers pre- sent). Plesiomorphy: (0) suckers absent. Apomor- phy: (1) suckers present [101]. Polarisation of the series is by functional outgroup comparison. 40. Mid-sclerite of sucker (suckers present). Plesi- omorphy: (0) absent. Apomorphies: (1) termin- ates in hook [92]; (2) flared or truncate [114]. Polarisation is by functional outgroup compari- son. 41. Posterior mid-sclerite (suckers present). Plesi-

Phylogeny and classification of the Monogenoidea 9

(ooo) A

(ioo) (2oo)

(010) (020) (030)

5 Fig. 5. Postulated transformation of number and distribution of hooks in the oncomiracidium of the Monogenoidea (diagrammatic): A, 16 marginal; B, 14 marginal; C, 14 marginal, 2 central; D, 12 marginal, 2 central; E, 10 marginal; F, 6 marginal; G, 4 marginal. Numbers in parentheses indicate the respective code each state received in the matrix (homologous series 28).

omorphic: (00) absent. Apomorphies: (10) rod- shaped (Fig. 8G,H,L,M) [163]; (01) plate-like (Fig. 8J,K) [118]. The derived states are thought to have evolved independently (coded by additive binary coding); polarisation is by functional out- group comparison. 42. Accessory sclerite (suckers present). Plesi- omorphy: (0) absent. Apomorphies: (1) parallel to mid-sclerite (Fig. 8B) [124]; (2) perpendicular to mid-sclerite (Fig. 8C) [126]. Polarisation is by functional outgroup comparison. 43. Lateral sclerites (suckers present). Plesiomor- phy: (0) absent [102]. Apomorphy: (1) present [89]. Polarisation is by functional outgroup com- parison.

44. Number of lateral sclerites (when present). Plesiomorphy: (0) one pair [88]. Apomorphies: (1) two pairs (Fig. 8A-C,E-G,L,M) [117]; (2) two pairs, posterior pair broken (Fig. 8D,H,I) [119, 152, 165]; (3)two pairs, anterior pair distally fused, distal posterior pair fused (Fig. 8J,K) [121]. Transformation of this series is provided in Fig. 10. 45. "Crochet en fl~au" (oncomiracidium). Plesi- omorphy: (0) absent [109]. Apomorphy: (1) pre- sent [87]. The series is polarised by functional outgroup comparison.

Llewellyn (1963) considers the "crochet en fl6au" homologous with hooks (Fig. 6 in Llewel- lyn, 1963), while other workers (Gusev, 1978b,

10 W.A. Boeger and D.C. Kritsky

:Sh

(ioooo> C (10001)

,00 , , , , .0000 \

(50000) (02000) (99919) 6

Fig. 6. Postulated transformation of number and distribution of hooks in the adult of the Monogenoidea (diagrammatic): A, 16 marginal; B, 14 marginal; C, 14 marginal, 2 central; D, 12 marginal, 2 central; E, 2 marginal; F, 10 marginal, 2 central, 4 dorsal; G, 2 marginal, 4 in each of two lateral haptoral lobes; H, absent; I, 8 marginal, 2 central, 4 dorsal. Numbers in parentheses indicate the respective code each state received in the matrix (homologous series 29).

Malmberg, 1990, among others) classify this scler- ite as a true anchor. Since there is no definitive evidence to resolve the question, we incorporated three hypotheses into independent analyses as fol- lows: (1) "crochet en fl6au" was considered hom- ologous to a hook; (2) "crochet en fl6au" was

considered homologous to an anchor; and (3) "crochet en fl6au" was considered a "de novo" sclerite. All three were equally supported. We treat the "crochet en fl6au" as a "de novo" struc- ture while recognising that unequivocal evidence for its origin is lacking.

Phylogeny and classification of the Monogenoidea 11

7 Fig. 7. Hook types (diagrammatic): A, unhinged; B, hinged.

In the present analysis, the existing term "cro- chet en fl6au" is used for all forms of the so-called "posteriormost hooks" of Llewellyn (1963, fig. 6) to indicate our proposals of homology and "de novo" development of the sclerite in the Mono- genoidea. 46. "Crochet en fldau" in adult (present in onco- miracidium). Plesiomorphy: (0) present. Apomor- phy: (1) absent [132, 139]. Polarisation is by func- tional outgroup comparison. 47. Shape of "crochet en fl(au" (present in onco- miracidium and/or adult). Plesiomorphy: (00) hook-like (Fig. 11A) [86, 171]. Apomorphies: (10) plectanocotylid (Fig. 11B) [120]; (01)microcotylid (Fig. 11C) [123]; (02) gastrocotylid (Fig. l lD) [127]. Polarisation is by functional outgroup com- parison (coded by mixed coding).

Phylogeny and revised classification of the Mono- genoidea

The cladogram, based on the present analysis and depicting phylogenetic relationships of families of the Monogenoidea, is presented in Figs 13-18; an abridged hypothesis for the class and ordinal taxa is offered in Fig. 12. The consistency index (CI = 57.3%) was the highest obtained for hypotheses

produced through the PAUP analysis utilising the 47 homologous series. Monophyly of the class is supported by seven synapomorphies: (1 & 2) adult and oncomiracidium with two pairs of eyes; (3 & 4) adult and oncomiracidium with 16 hooks that are marginal in the haptor; (5 & 6) presence of anchors, a single pair ventral in the haptor. Al- though not used in the analysis, the presence of three rows of ciliary epidermal bands in the onco- miracidium represents the seventh synapomorphy for the class (see Ehlers, 1985; Brooks, 1989b).

While a strict bifurcating classification based on phylogeny may be the most informative and, therefore, preferable (e.g. Brooks, 1989b), the number of taxonomic levels required for such a system quickly becomes cumbersome when dea- ling with large terminal taxa such as the Mono- genoidea. Therefore, while the present analysis could potentially be used to support other sys- tems, our proposed classification including divi- sion of the Monogenoidea into the three sub- classes, the Polyonchoinea, Polystomatoinea and Oligonchoinea, as suggested by Lebedev (1988), is based on the hypothesised sequence of appear- ance of respective taxa within the class: it appears to be a reasonably efficient system while fur- nishing evolutionary information about the group.

The Polyonchoinea is supported by seven syna- pomorphies, of which presence of a ventral mouth, reduced numbers of subsurface sperm microtubules, and 14 marginal and two central hooks in both the oncomiracidium and adult hap- tors, appear the most significant. The sister re- lationship of the Polystomatoinea and Oligonch- oinea is based on six synapomorphies concerning the presence and associations of multiple testes, the genito-intestinal canal, haptoral suckers and the "ductus vaginalis." Monophyly of the Polysto- matoinea and Oligonchoinea is supported by one and seven synapomorphies, respectively. The pro- posed classification for the familial taxa of Mono- genoidea and coordinated with our phylogenetic hypothesis follows:

12 W.A. Boeger and D.C. Kritsky

7 c~

c~ I m

o - .= ~ "~ "~

~ - - ~ - - , j ~ ~ ~ = ~ ~-~-~o • _ ~ ~. .-~ ~ ,- 6

0 ~ ~ .-- ~ . ~

" 0 . ' - - "~ . ~= 0 ¢~ ~ "~

m.~ ~ . ~ ' ~ ~,_~ ,-~ ~ "~ ~..- ~ ~ ~.,-- ~ ~ - ~

~ . ~ ~ ~ ,~' 0 '~, "~

0 ~ 0.,

, o ~ - - ~ ~ ' t = ~ ~ ~

~ , ~ ' ~ "~ ~ ~ " " ~ ~ ~ _ ~

" 7 , - - -

i

0 ,~

. ' . -

T H R E E P A I R S (00000)

P h y l o g e n y a n d c l a s s i f i c a t i o n o f t h e M o n o g e n o i d e a

, O N E P A I R (01000)

13

~ M U L T I P L E " M I C R O C O T Y L I D " (20000)

MULTIPLE "GASTROCOTYLID" (10100)

FOUR PAIRS

(10000) ~-"-'--'-'-~ MULTIPLE "DICLIDOPHORID" (10010)

MULTIPLE "FIRE TONG" (10001) 9 Fig. 9. Postulated transformation of number and type of haptoral suckers. Numbers in parentheses indicate the respective code each state received in the data matrix (homologous series 38).

(0)

/ )

(1) 1

Fig. 10. Postulated transformation of lateral sclerites in hapto- ral suckers (diagrammatic). Numbers in parentheses indicate the respective code each state received in the data matrix (homologous series 44).

J B (1o)

11 ~C (01)

Fig. 11. Proposed transformation of types of "crochet cn fldau" in the monogcnoidcan haptor (diagrammatic): A, hook like; B, plcctanocotylid; C, microcotyiid, D, gastrocotylid. Numbers in parentheses indicate the respective code each state received in the data matrix (homologous series 47).

14 W.A. Boeger and D.C. Kritsky

Polyonchoinea

Dactylogyridea

7 , I "~ -~ I "~ - "~ o -~ I ' I - ~ ~ °

!t -16

33,3 ,

Polystomatoinea

I .'2.

O t ~

I I .'2_

I o h e-.

Oligonchoinea

Mazocraeidea f

6 6

i ~ 6 s e 8

~ 153

123

17-100

12

Fig. 12. Abridged hypothesis for the evolutionary history of the subclass and ordinal taxa comprising the Monogenoidea. Slashes with numbers refer to postulated evolutionary changes as indicated in the character analysis and Addendum I.

Class Monogenoidea Bychowsky, 1937

Subclass Polyonchoinea Bychowsky, 1937 Order Monocotylidea Lebedev, 1988

Family Monocotylidae Taschenberg, 1879 Family Loimoidae Price, 1936

Order Capsalidea Lebedev, 1988 Family Acanthocotylidae Price, 1936 Family Capsalidae Baird, 1853 Family Dionchidae Johnston & Tiegs, 1922

Order Montchadskyellidea Lebedev, 1988 Family Montchadskyellidae Bychow- sky, Korotajeva & Gusev, 1970

Order Gyrodactylidea Bychowsky, 1937 Family Gyrodactylidae Van Beneden & Hesse, 1863 Family Anoplodiscidae Tagliani, 1912 Family Bothitrematidae Price, 1936 Family Tetraonchoididae Bychowsky, 1951

Order Dactylogyridea Bychowsky, 1937 Suborder Calceostomatinea Gusev, 1977

Family Calceostomatidae Parona & Perugia, 1890

Suborder Neodactylodiscinea new suborder Family Neodactylodiscidae Kamegai, 1972

Suborder Amphibdellatinea new suborder

Phylogeny and classification of the Monogenoidea 15

.g.,~ c~

Z • ~ m

-~ "n o .~, :~, ~ ..~ • ,.~ . ,~ 0

+a +a ~ 0 0 o ~ o o o ~ ,--. ~ r j 0

0 ~ ~ 5z • .~ ~ c~ •

"", <X3-8~ <,o8~3-,o, ,,]x,~ / ,, ",, " , , , \ ,, ", ~ ~ ~ 1 0 1 , 1 0 2 V / "

~ ~ 93-96"~~ "117

Urn-81 4

13 Fig. 13. Portion of cladogram depicting the evolutionary hypothesis for the Polyonchoinea, Polystomatoinea and basal families of the Oligonchoinea. Slashes with numbers refer to postulated evolutionary changes as indicated in the character analysis and Addendum I; dashed lines indicate continuation to clades in Figs 14 and 16, respectively.

Family Amphibdellatidae Carus, 1885 Suborder Tetraonchinea Bychowsky, 1937

Family Tetraonchidae Monticelli, 1903 Family Neotetraonchidae Bravo- Hollis, 1968

Suborder Dactylogyrinea Bychowsky, 1937 Family Dactylogyridae Bychowsky, 1933 Family Pseudomurraytrematidae Krit- sky, Mizelle, & Bilqees, 1978 Family Diplectanidae Monticelli, 1903

Subclass Polystomatoinea Lebedev, 1986 Order Polystomatidea Lebedev, 1988

Family Polystomatidae Gamble, 1896 Family Sphyranuridae Poche, 1926

Subclass Oligonchoinea Bychowsky, 1937 Order Chimaericolidea Bychowsky, 1957

Family Chimaericolidae Brinkmann, 1942

Order Diclybothriidea Bychowsky, 1957 Family Diclybothriidae Price, 1936 Family Hexabothriidae Price, 1942

Order Mazocraeidea Bychowsky, 1937 Suborder Mazocraeinea Bychowsky, 1957

Family Plectanocotylidae Monticelli, 1903 Family Mazoplectidae Mamaev & Slipchenko, 1975 Family Mazocraeidae Price, 1936

Suborder Gastrocotylinea Lebedev, 1972, sedis mutabilis

Infraorder Anthocotylina new infraorder

16 W.A. Boeger and D.C. Kritsky

<

o -~ .~ ~ ~ ~ o ~ o • ¢ 0 ,.~ " ~ ~'~ . ~ 0

o,,,.. / / \ / " H-,.

19,20"~

, 1 4 x\

Fig. 14. Cladogram showing evolutionary relationships of the Monocotylidea, Capsalidea, Montchadskyellidea, Gyrodactylidea and Dactylogyridea (Polyonchoinea). Slashes with numbers refer to postulated evolutionary changes as indicated in the character analysis and Addendum I; dashed lines indicate continuation from/to the clades in Fig 13 and 15, respectively.

Family Anthocotylidae Price, 1936 Infraorder Gastrocotylina Lebedev, 1972

Family Pseudodiclidophoridae Yama- guti, 1965, incertae sedis

Superfamily Protomicrocotyloidea John- ston & Tiegs, 1922, sedis mutabilis

Family Protomicrocotylidae Johnston & Tiegs, 1922 Family Allodiscocotylidae Tripathi, 1959 Family Pseudomazocraeidae Lebedev, 1972 Family Chauhaneidae Euzet & Trilles, 1960

Superfamily Gastrocotyloidea Price, 1943, sedis mutabilis

Family Bychowskycotylidae Lebedev, 1969 Family Gastrocotylidae Price, 1943 Family Neothoracocotylidae Lebedev, 1969 Family Gotocotylidae Yamaguti, 1963

Suborder Discocotylinea Bychowsky, 1957, sedis mutabilis

Family Discocotylidae Price, 1936 Family Diplozoidae Tripathi, 1959 Family Octomacridae Yamaguti, 1963

Suborder Hexostomatinea new suborder Family Hexostomatidae Price, 1936

Suborder Microcotylinea Lebedev, 1972 Superfamily Microcotyloidea Taschen- berg, 1879

4-~ 0 0

~, o o 0

67'68" 6560 .~6~ .....

~ -,~ ~ :~ , ~ "C~

0

~ o

15 Fig. 15. Cladogram depicting phylogenetic hypothesis of the Dactylogyridea (Polyonchoinea). Slashes with numbers refer to postulated evolutionary changes as indicated in the charac- ter analysis and Addendum I; the dashed line indicates con- tinuation from the clade in Fig. 14.

Family Axinidae Monticelli, 1903 Family Diplasiocotylidae Hargis & Dillon, 1965, sedis mutabilis Family Heteraxinidae Unnithan, 1957, sedis mutabilis Family Microcotylidae Taschenberg, 1879, sedis mutabilis

Superfamily Allopyragraphoroidea Ya- maguti, 1963, sedis mutabilis

Family Allopyragraphoridae Yama- guti, 1963

Superfamily Diclidophoroidea Cerfon- taine, 1895, sedis mutabilis

Family Diclidophoridae Cerfontaine, 1895

Superfamily Pyragraphoroidea Yama- guti, 1963, sedis mutabilis

Family Pterinotrematidae Caballero & Bravo-Hollis, 1955 Family Rhinecotylidae Lebedev, 1979, sedis mutabilis

Phylogeny and classification of the Monogenoidea 17

Family Pyragraphoridae Yamaguti, 1963, sedis mutabilis Family Heteromicrocotylidae Unni- than, 1961, sedis rnutabilis

Taxa incertae sedis: Sundanonchidae Malmberg, 1990 [Polyonchoinea]; Iagotrematidae Mafi6-Gar- z6n & Gil, 1962 [Polyonchoinea]; Microbothriidae Price, 1936 [Monogenoidea].

The Sundanonchidae was proposed by Malmberg (1990), because of the reported presence of dorsal and ventral pairs of anchors and 16 haptoral hooks that were assumed to be "hinged" in the three species of Sundanonchus described by Lim & Fur- tado (1985). Original descriptions and drawings of the haptors and haptoral sclerites of the three species provided by Lira & Furtado (1985) do not allow determination of some important character states of the haptor and haptoral sclerites. As a result, we did not include this family in the analysis.

Specimens of Iagotrema uruguayensis Mafi6- Garz6n & Gil, 1962 were not available for study, which precluded inclusion of the Iagotrematidae in the analysis. Published accounts concerning the morphological features of this species, and both Euzetrema knoepffieri Combes, 1965 and E. cau- casica Timofeeva & Sharpilo, 1979, the only other species in the rarely, suggest possible polyphyly. According to the original description, I. uruguay- ensis lacks a vagina and possesses a haptor armed with 14 hooks (all marginal) and two pairs of anchors, and a sclerotised male copulatory organ with accessory piece (Mafi6-Garz6n & Gil, 1962). Euzetrema species are reported with double vagi- nae, a spined male copulatory pouch, and a haptor armed with 16 hooks (14 marginal, 2 central) and two pairs of anchors (Combes, 1965; Timofeeva & Sharpilo, 1979). If the family is monophyletic, it probably has its origins within the Polyonchoinea based on the presence of a sclerotised male cop- ulatory organ in the former species.

Monophyly of the Microbothriidae is also ques- tionable. Not only are species currently assigned to the family morphologically diverse, but the family has historically been used as a "catch all"

18 W.A. Boeger and D.C. Kritsky

2; °

° t - I 0 .,_b

• o

o I~ c} I:m., " ~

• r , , , i

<

O

/

". ",~149/'147 \ 162",,. / / / ,"

~ 153

./"' 16 /

/ /

+, /

Fig. 16. Cladogram showing phylogenetic relationships of the Gastrocotylinea, Mazocraeinea, Hexostomatinea and basal families of the Microcotylinea (Oligonchoinea, Mazocraeidea). Slashes with numbers refer to postulated evolutionary changes indicated in the character analysis and Addendum I; dashed lines indicate continuation from/to clades in Figs 13, 17 and 18, respectively.

taxon for species lacking haptoral sclerites. For example, Enoplocotyle Tagliani, 1912 and Ano- plodiscus Sonsino, 1890 were previously con- sidered members of this family but since have been transferred to other familial taxa within the Monogenoidea (Acanthocotylidae and Anoplodi- scidae, respectively). Due to the lack of infor- mation on character states (especially on larval characters) and to its possible polyphyly, the Mic- robothriidae was not included in the analysis and is considered incertae sedis within the Monogen- oidea.

Remarks on specific taxa

The following remarks relate to our observations of specimens during the character analysis and/or

to the status of specific taxa in light of new or previously published information. Individual diag- noses of new ordinal taxa proposed above are not provided; however, the number and identity of hypothesised synapomorphies for each taxon pro- posed or considered in the study are identified in the cladogram and character analysis.

Acanthocotylidae Monticeili, 1903. Malmberg & Fernholm (1989) divided the Acanthocotylidae into three subfamilies, the Myxinidocotylinae Malmberg & Fernholm, 1989, Lophocotylinae Yamaguti, 1963 and Acanthocotylinae, and, in so doing, excluded the apparently related Enoploco- tile from the family. Although Malmberg & Fernholm (1989) referred to E. minima Tagliani, 1909 as an "enoplocotylid," no reference to eleva-

Phylogeny and classification of the Monogenoidea 19

o

o n3 o o 0~ O~ o .~ 0 "0 0 . ~

.~ O o o o ~: "o o o o °

o ~ ,~ ~ .~ o -0 o ~c~

0 Z m m m

1 2 5 - 1 2 7 ~ _ _

x

Xx x

x

"0 oF,, ,I

o m

o • r. .* b , ]

o~ o ~c~

17

Fig. 17. Cladogram depicting phylogenetic relationships of the families comprising the Gastrocotylinea (Oligonchoinea, Mazocraei- dea). Slashes with numbers refer to postulated evolutionary changes as indicated in the character analysis and Addendum I; the dashed line indicates continuation from the clade in Fig 16.

tion of the subfamily was made until Malmberg (1990) proposed the Enoplocotylidae for this spe- cies. Malmberg's (1990) proposal was premised primarily on haptoral armature and the absence of a pseudohaptor. Based on morphology of sub- adult and adult specimens, Kearn & Vasconcelos (1979) discount possibilities that E. minima shares relationship with microbothriids, monocotylids or calceostomatids as proposed by earlier authors. They suggest two possibilities regarding its origin: (1) that Enoplocotyle is an acanthocotylid that arrives at sexual maturity (adulthood) before de- velopment of some diagnostic features of the fam- ily (i.e. the pseudohaptor); or (2) that the species emerged in the family's history before evolution- ary development of the pseudohaptor in other acanthocotylids. While our phylogenetic analysis does not directly address the evolution of the

pseudohaptor, functional outgroup comparison concerning its presence or absence supports their latter scenario. Our character and phylogenetic analyses justify return of E. minima to the Acan- thocotylidae.

Capsalidae Baird, 1853. Determination of approp- riate character states in homologous series con- cerning haptoral structures for capsalids is prob- lematical. Most of the problem rests with classification of the different sclerites found in various capsalid groups. None, one, two and three pairs of anchors have been reported in members of the family (see Yamaguti, 1963; Price, 1939a); and hook number and distribution (homologous series 28 and 29) vary from 14 marginal to 14 marginal + 2 central, depending on investigator classification of the so-called "accessory sclerite"

20 W.A. Boeger and D.C. Kritsky

,• o ~ o "0 ~ ~ ~' o

1 6 4 ~ "167 ~72 ,173

U 168

18 r S

Fig. 18. Cladogram depicting the evolutionary relationships of the terminal families of Microcotylinea (Oligonchoinea, Mazo- craeidea). Slashes with numbers refer to postulated evolution- ary changes as indicated in the character analysis and Adden- dum I; the dashed line indicates continuation from the clade in Fig. 16.

of Kearn (1963a). Kearn's (1963a,b) respective descriptions of the haptoral development of En- tobdella soleae (van Beneden & Hesse, 1863) and Capsala martinierei Bosc, 1811 suggests homology of the centrally-located "accessory sclerite" with the central pair of hooks of the 14 marginal + 2 central hook-state, an idea shared by Llewellyn (1968, 1970). Present evaluation of morphological states in sister groups supports this notion on hom- ology and that one pair of anchors is primitive for the Capsalidae; the second pair of anchors of some species of Capsalidae apparently developed "de novo".

Dionchidae Johnston & Tiegs, 1922. The sister relationship of the Dionchidae to the Capsalidae is supported by four synapomorphies, the most significant of which being the presence of double testes and a muscular, elongate male copulatory organ. Although Timofeeva (1988) considered the centrally located haptoral sclerites of the Dionchi- dae to be the modified central pair of hooks in the "14 marginal + 2 central" hook-state based

on a study of haptoral development in dionchid oncomiracidium, we postulate that the Dionchi- dae lost the central pair of hooks and retained the primitive "one-pair of anchors, ventral in haptor". Both explanations are equally parsimonious and do not affect cladogram topology or consistency. However, if indeed the central haptoral sclerites of dionchids are modified central hooks, the Cap- salidae and Dionchidae would share the additional synapomorphy, "modification of the 2 central hooks." Finally, Justine's (1991) classification of sperm types in monogenoideans provides ad- ditional support for the sister relationship between these two families. Members of both share his "Type 2a" sperm pattern characterised by a bead- like mitochondrion and "loss" of microtubules in the zone of differentiation during spermiogenesis (Justine et al., 1985; Justine & Mattei, 1986, 1987).

Montchadskyellidea Lebedev, 1988. Lebedev (1988) proposed the Montchadskyellinea (Montchadskiellinea in Lebedev, 1988, an appar- ent unjustified correction in spelling of the type genus) for the monotypic Montchadskyella By- chowsky, Korotajeva & Nagibina, 1970, and placed it in the Monocotylidea, while recognising significant morphologic distinction between M. intestinale Bychowsky, Korotajeva & Nagibina, 1970 and other monocotylideans. Phylogenetic analysis supports an independent origin of the Montchadskyellidae within the Polyonchoinea. Therefore, we propose removing the taxon from the Monocotylidea and elevating Lebedev's sub- order to the status of order.

Gyrodactylidea Bychowsky, 1937. Portions of our proposed configuration of the Gyrodactylidea have been suggested previously by Bychowsky, Gusev, & Nagibina (1965), Ogawa & Egusa (1981) and Gerasev (1987), all of whom supported their ideas in part by the common occurrence of hinged ("gyrodactylid") hooks. Malmberg (1990) proposed the Articulonchoinea to include all fam- ilies (the Acanthocotylidae, Enoplocotylidae, An- oplodiscidae, Gyrodactylidae, Ooegyrodactyli- dae, Tetraonchoididae and Bothitrematidae) with

Phylogeny and classification of the Monogenoidea 21

members having "hinged" hooks. Our analysis indicates that the Articulonchoinea is polyphy- letic, in that the Acanthocotylidae, including the Enoplocotylidae, belongs in the Capsalidea.

Gyrodactylidae Van Beneden & Hesse, 1863. Among characters supporting the position of this family in the Monogenoidea are the structure of the sperm cell (Kritsky, 1976), the looping of the vas deferens around the left cecum (Kritsky, 1970), and the presence of an accessory piece (postulated homology by Kritsky & Boeger0 1991). The sister relationship of the Gyrodactyli- dae with the Anoplodiscidae, Tetraonchoididae and Bothitrematidae is supported by the morpho- logical similarity of the haptoral sclerites (bars, anchors and/or hooks).

Because of its viviparous mode of reproduction, relationships of the Gyrodactylidae have pre- viously been difficult to determine. However, re- cognition of oviparity in some gyrodactylids by Harris (1983) clearly established that viviparity was a secondary characteristic and therefore could not be used to determine relationship of the family with others in the class.

Harris (1983) proposed the Ooegyrodactylidae for oviparous gyrodactylids. However, oviparity is plesiomorphic and as such should not be used as a diagnostic character for a family. Kritsky & Boeger (1991) were unable to identify synapo- morphies for the Ooegyrodactylidae, suggesting that the taxon is paraphyletic. We tentatively con- sider the Ooegyrodactylidae a junior synonym of the Gyrodactylidae until appropriate synapo- morphies are identified.

Anoplodiscidae Tagliani, 1912. The sister relation- ship of the Anoplodiscidae with the Tetraonchoid- idae and Bothitrematidae was suggested by Ogawa & Egusa (1981), who overturned place- ment of Anoplodiscus in the Microbothriidae. Al- though adults of Anoplodiscus species lack haptoral sclerites, its oncomiracidium possesses 16 marginal hinged "gyrodactylid" hooks. Species of Anoplodiscus also share the synapomorphy, sac- like gut, with the Bothitrematidae and Tetraon-

choididae supporting its proposed position in the Gyrodactylidea,

Dactylogyridea Bychowsky, 1937. Our proposal for composition of this order differs from most previous accounts by the inclusion of the Amphib- dellatidae (Amphibdellatinea) plus the Tetraon- chidae and Neotetraonchidae (Tetraonchinea). Lebedev (1988) included species representing the Dactylogyridae, Diplectanidae, Pseudomurraytre- matidae and Neodactylodiscidae (Dactylogyrinea) plus the Calceostomatidae (Calceostomatinea) in the order.

Justine (1991) proposed the apparent ordinal epithet, Monoaxonematidea, for a group of po- lyonchoinean taxa having spermatozoa with single axonemes as its synapomorphy. His (1991) configuration of the Monoaxonematidea is identi- cal to that of the Dactylogyridea (sensu nobis). Recently, Justine et al. (1991) reported that a spe- cies of Tetraonchoididae also has spermatozoa with single axonemes. Incorporation of these new data into the matrix does not change the cladog- ram topology. Single axonemes in polyonchoine- ans clearly represent evolutionary loss of one ax- oneme from the primitive "two axoneme" state. Since homologies are often difficult to determine when character states constitute loss of structure (see Kritsky & Kulo, 1992), Justine's ta×on based only on sperm structure would be polyphyletic if the Tetraonchoididae were included within it. Therefore, we recommend that the Monoaxonem- atidea be rejected as a junior synonym of the Dactylogyridea and/or as an unnatural taxon.

Neodactylodiscinea new suborder. The Neodac- tylodiscidae had been placed in the Dactytogyri- nea apparently because of the reported presence of 14 haptoral hooks (see Lebedev, 1988). Our study of paratypes of Neodactylodiscus latimeris Kamegai, 1971, revealed that the species pos- sesses 16 hooks distributed similarly to those of the Tetraonchinea (10 marginal, 2 central, 4 dor- sal). Thus, placement of the family in the Dactyl- ogyrinea is unjustified and a new suborder consis- tent with our analysis and hypothesis is proposed.

Although Kamegai (1971) reported that Neo-

22 W.A. Boeger and D.C. Kritsky

dactylodiscus latimeris lacks an accessory piece, we observed a structure paralleling the male cop- ulatory organ in one specimen. Since we could not confirm its presence in the other specimens available for study, we decided to consider the state unknown for the family. The analysis, how- ever, suggests that it is likely that an accessory piece is present in this species.

Amphibdellatinea new suborder. The present analysis indicates that the Amphibdellatidae had an independent origin within the Dactylogyridea. A new suborder is proposed to accommodate the family.

Amphibdellatidae Carus, 1885. Previous accounts of the morphology of amphibdellatids indicate that the vas deferens is intercaecal. Our initial hypotheses suggested that this pathway would be a homoplasy (reversal) for the family since family taxa of its sister group and those of the Gyrodac- tylidea and Montchadskyellidea possess a vas de- ferens looping the left intestinal caecum. How- ever, specimens of Amphibdella Chatin, 1874 and Amphibdelloides Price, 1937 we studied clearly showed that the vas deferens loops the left caecum in accordance with the condition found in its sister groups and predicted by initial phylogenetic analy- ses.

Similar erroneous descriptions of the germar- ium as intercaecal exist for species of Amphibdel- loides. Examination of specimens of A. maccal- lumi (Johnston & Tiegs, 1922) showed that this species shares the characteristic "germarium/ovid- uct looping the right intestinal caecum" with members of Amphibdella.

Dactylogyridae Bychowsky, 1933. The Heterotesi- idae Euzet & Dossou, 1979, Ancyrocephalidae Bychowsky & Nagibina, 1978 and Pseudodac- tylogyridae Le Brun, Lambert & Justine, 1986 were reduced to subfamilies of the Dactylogyridae by Kritsky & Boeger (1989) in their test of mono- phyly of the Ancyrocephalidae using cladistic analysis. Their recommendations for subfamilial status of the three named taxa are accepted herein.

Chimaericolidea Bychowsky, 1957. Many ques- tions have been raised concerning homology and origin of the haptoral sclerites of the Chimaericoli- dea, Diclybothriidea and Mazocraeidea. Regard- ing those of the Chimaericolidea, Beverley-Bur- ton et al. (in press) reported that the oncomiracidial haptor of Callorhynchicola multitesticulatus Manter, 1955 possesses 14 hooks (each with a "riotous"), one pair of anchors and one pair of "slender, almost featureless" sclerites. In the adult haptor, 14 hooks with a "domus", one pair of anchors and a pair of larger hook-like sclerites lacking a "domus" are present; the larger hook-like sclerites are developed from the fea- tureless sclerite of the oncomiracidial haptor (Be- verley-Burton et al., in press). These investigators were reluctant to classify the "featureless sclerite" of the oncomiracidial haptor and the hook-like sclerite lacking a "domus" as either a hook or anchor. Similarly, our analysis did not resolve sclerite classification in chimaericolideans. How- ever, it does support homology of the hook-like sclerite of the adult haptor with the "crochet en fl6au" of other oligonchoineans (character series 45).

Although one marginal hook pair of the onco- miracidium of C. multitesticulatus apparently mi- grates to a submarginal position during develop- ment to the adult stage (Beverley-Burton et al., in press), we do not consider the hook distribution of the adult of this species to be homologous to the "12 marginal + 2 central" state of the Calceo- stomatidae, where in contrast, the central hooks are located near the centre of the haptor. Thus, both the larval and adult haptors of chimaericoli- deans are coded to have 14 hooks (marginal), which represents a loss of one pair from the primi- tive state (see character series 28, 29).

Beverley-Burton et al. (in press) reported for the first time that hooks persist within the haptoral suckers in adults of C. multitesticulatus. This ap- parent primitive feature is shared with the Poly- stomatoinea and provides evidence in support of proposed haptoral-sucker homology and of the basal position of the origin of the Chimaericolidea in oligonchoinean phylogeny.

Bychowsky (1957) suggested homology of the

Phylogeny and classification of the Monogenoidea 23

mid-sclerite of the sucker of chimaericolideans with those of the Diclybothriidea based on his observation of a small hook at the sclerite tip in members of both orders. This homology is sup- ported by comparative histochemistry (Lyons, 1966) and by our parsimony analysis, although we could not confirm the presence of the hooked tip in the specimens of Chimaericola leptogaster, (Leuckart, 1830), C. colliei Beverley-Burton et al., 1991 and Callorhynchicola multitesticulatus we examined. The tip of the midsclerite of Chimaeric- ola ogilbyi Beverley-Burton et al., 1991 is trifid (Beverley-Burton et al., 1991) and as such is remi- niscent of the mid-sclerite of some mazocraeidean species. Despite histochemical differences re- ported by Lyons (1966), homology of the mid- sclerites of chimaericolideans and mazocraeideans is also supported by the present parsimony analy- sis.

Mazocraeinea Bychowsky, 1957. Based on com- parative morphology of the haptoral sucker, the male copulatory organ and genital atrium, Ma- maev & Slipchenko (1975) presented a hypothesis on the evolutionary relationships of the familial taxa of the Mazocraeinea (sensu nobis), in which they considered the plectanocotylids sister to the mazoplectids. Our hypothesis differs from theirs by suggesting sister-group relationship of the Ma- zoplectidae and Mazocraeidae. In the Mazocraei- dae and Mazoplectidae, fusion of the antero-lat- eral and distal postero-lateral sclerites of the haptoral suckers represent synapomorphies sup- porting our phylogenetic hypothesis. While Ma- maev & Slipchenko (1975) apparently considered the presence of a spined copulatory organ in mem- bers of the Mazoplectidae and Plectanocotylidae, the synapomorphy supporting their configuration, spined copulatory organs, also occur in members of other mazocraeidean families (e.g. Gastrocotyl- idae, Pseudodiclidophoridae), suggesting the op- posite polarisation. Therefore, absence of spines of the copulatory organ in the Mazocraeidae should likely be considered an autapomorphic state; as such, spination of the copulatory organ provides no information to determine relationship at this subordinal level. Similarly, the genital at-

rium does not provide evolutionary information for the group since the unspined state found in species of Plectanocotylidae is autapomorphic.

Gastrocotylinea Lebedev, 1972. We recognise two infraorders within the Gastrocotylinea: the mono- typic Anthocotylina new infraorder and Gastroco- tylina Lebedev, 1972. Lebedev (1988) considered the Anthocotylidae aligned with families of the Discocotylidea (sensu nobis) and Diclidophori- dae. Our transfer of the family to the new in- fraorder within the Gastrocotylinea is supported by our hypothesised homology of the accessory sucker sclerite of the anthocotylids with those of other gastrocotylineans. This homology was pre- viously suggested by Lebedev (1976), who con- sidered arguments for placing the Anthocotylidae within or outside the Gastrocotylinea. Our analy- sis suggests that this sclerite was parallel with the mid-sclerite of the sucker in the immediate ances- tor of the Anthocotylina and Gastrocotylina, and that a change to perpendicular to the mid-sclerite occurred in the common ancestor of families we place in the Gastrocotylina.

Gastrocotylina Lebedev, 1972. This infraorder is divided into two superfamilies, the Gastrocotylo- idea Price, 1943 and the Protomicrocotyloidea Johnston & Tiegs, 1922. Lebedev (1972, 1988) recognised the Gotocotyloidea Yamaguti, 1963, containing the Gotocotylidae and Allodiscocotyli- dae, and the Gastrocotyloidea, with the remaining families of the suborder (sensu nobis). Lebedev's configuration is rejected, since it renders the Gas- trocotyloidea paraphyletic. The Protomicroco- tyloidea (sensu nobis) comprises the Protomicroc- otylidae, Allodiscocotylidae, Chauhaneidae and Pseudomazocraeidae, and is supported by two synapomorphies, testes lying anterior to the germ- arium and a ventro-lateral "ductus vaginalis".

We were unable to resolve the position of the Pseudodiclidophoridae Yamaguti, 1965, and as a result consider its position incertae sedis within the Gastrocotylina. Nonetheless, comparative morphology of the male copulatory organ in spe- cies of Pseudodiclidophoridae and Bychowskyco-

24 W.A. Boeger and D.C. Kritsky

tylidae indicates that these families might share a common ancestor.

Hexostomatinea new suborder. Bychowsky (1957) incorporated the Hexostomatidae in the Mazocra- einea based, in part, on what he considered to be homologies between the middle sclerite of the hexostomatid sucker and portions of the "cap- sule" of mazocraeids. Subsequent revisers have retained the Hexostomatidae in the Mazocraeinea (Gusev, 1977; Mamaev & Lebedev, 1979; Le- bedev, 1988). Our analysis reveals characters that do not corroborate this hypothesis. Hexostomat- ids exhibit a single mid-sclerite and two pairs of entire lateral sclerites in the sucker, an unarmed male copulatory organ and a mid-dorsal vagina, all of which would have to be considered homo- plasies if the family were retained in the Mazocra- einea. Therefore, we propose the new suborder to accommodate this family with an hypothesised independent origin within the Mazocraeidea.

Microcotylidae Taschenberg, 1879. This family is apparently polyphyletic. Thus, character states used in our analysis were determined exclusively from species of Microcotyle.

Allopyragraphoridae Yamaguti, 1963. Our study of specimens of Allomicrocotyla Yamaguti, 1965 and Allopyragraphorus Yamaguti, 1963 revealed many erroneous observations reported in the liter- ature concerning the morphology of allopyragra- phorids. Some of these errors were also detected by Mamaev & Parukhin (1981), whose paper should be referred to for character states. The second "ventrally curved hollow median sclerite" described by Yamaguti (1965) within the sucker of Allomicrocotyla onaga Yamaguti, 1965 represents the posterior mid-sclerite. In addition, the lateral sclerites in haptoral suckers of species of both genera are strongly flattened. Although the latter character is not included in the present analysis, it represents an autapomorphy of the family.

Diclidophoridae Cerfontaine, 1895. We incorpor- ated Macrovalvitrematidae and Anchorophoridae into the Diclidophoridae since recognition of the

former families would confer paraphyletic status to the Diclidophoridae. According to the evolu- tionary hypothesis of Mamaev (1976), both the Macrovalvitrematidae and Anchorophoridae have their origins within the Diclidophoridae and share common ancestors with separate diclidophorid genera. While not within the scope of the present study, phylogenetic analysis of all genera compris- ing the Diclidophoridae sensu lato will undoubt- edly support proposal of new family-group taxa with acceptance of the Anchorophoridae and Ma- crovalvitrematidae.

Pterinotrematidae Caballero & Bravo-Hollis, 1955. Proposal of higher taxa based on unique, sometimes highly derived, characters is frequently misleading and may result in unnatural taxa lack- ing evolutionary support (see Kritsky & Boeger, 1989; Kritsky & Kulo, 1992). Pterinotrematids have been afforded a status of order within the Monogenoidea by Mamaev & Lebedev (1979) and Lebedev (1988), apparently based on autapo- morphic characters associated with the highly modified sucker sclerites. However, acceptance of the order disregards other characters of the sucker sclerites (Fig. 8M) that indicate relationship with diclidophoroids, allopyragraphoroids and pyrag- raphoroids. The double rod-shaped mid-sclerite (present in the Pterinotrematidae) represents the synapomorphy for the terminal three superfamil- ies of Microcotylinea; in pterinotrematid species, all lateral sclerites are present but reduced near the articulation of the two mid-sclerites; and the Pterinotrematidae share the fire-tong sucker with the terminal three families in the clade.

Characters that suggest "primitiveness" of the Pterinotrematidae are homoplasies. The scler- otised "filamentous cirrus" of pterinotrematids apparently represents modified spines that are not homologous to the tubular male copulatory organs of polyonchoineans. In addition, our analysis indi- cates that retention of hooks in the adult haptor of pterinotrematids (an apparent primitive fea- ture) was likely derived from an oligonchoinean ancestor (with two ventral haptoral hooks in the adult haptor) as a result of loss of ability to shed hooks during maturation.

Phylogeny and classification of the Monogenoidea 25

Heteromicrocotylidae Unnithan, 1961. Although previously described as single, our study of the midsclerite of available specimens of Heteromicro- cotyla Yamaguti, 1953 clearly showed their double nature; double mid-sclerites represent the synapo- morphy for the terminal three superfamilies of the Microcotylinea, of which Heteromicrocotylidae is clearly a member. An autapomorphy for the Het- eromicrocotylidae (not used in our analysis) in- cludes the presence of an "accessory copulatory apparatus" lying on the mid-ventral surface an- terior to the genital atrium and pore (see Rohde, 1977).

Discussion

While our phylogenetic analysis justifies modifi- cation of contemporary classifications of the "monogenetic flukes" at lower taxonomic levels, it supports the division of the group into subordi- nate taxa as proposed in the two primary systems currently in use, i.e. that of Bychowsky (1937, 1957) and that of Janicki (1921) and Fuhrmann (1928). We chose to adopt and revise the classifi- cation of Bychowsky as modified by Lebedev (1988), since this system is less cumbersome when dealing with numerous terminal taxa while still providing evolutionary information about the group. The classification offered herein is not a strict bifurcating system but is based on the hypo- thesised sequence of emergence of family-group taxa during the evolutionary history of the Mono- genoidea.

Lebedev (1988) proposed the Polystomatoinea for the polystomatids and sphyranurids, which By- chowsky (1937, 1957) considered to be "lower Monogenoidea" that he placed in the Polyopistho- cotylinea Odhner, 1912, of the Gyrodactylidea. Bychowsky's proposal of sister-group relationship of the polystomatoineans and gyrodactylineans was based on plesiomorphic characters associated with the haptor (presence of 16 hooks, marginal), which confounded his classification and masked actual lineages. Based on our analysis, Lebedev (1988) was justified in proposing the Polystomato- inea, although the contention that his new sub-

class was an "intermediate" between the so-called "higher" and "lower" monogenoideans may be questioned. Most, if not all, characters that the Polystomatoinea share with the Polyonchoinea are plesiomorphic, while six synapomorphies are shared between it and the Oligonchoinea.

In his revision of the Polyonchoinea, Lebedev (1988) recognised the Tetraonchidea Bychowsky, 1957 to include the Tetraonchidae, Amphibdellat- idae, Tetraonchoididae and Bothitrematidae. Since our analysis indicates that this taxon is poly- phyletic, we incorporate the Tetraonchidae (along with the Neotetraonchidae) within the suborder Tetraonchinea of the Dactylogyridea. The Am- phibdellatidae and the Neodactylodiscidae (the latter assigned by Lebedev, 1988, to the Dactylo- gyrinea) also have independent origins within the Dactylogyridea and in our revision are assigned to new subordinal taxa, the Amphibdellatinea and Neodactylodiscinea, respectively. The remaining families, the Tetraonchoididae and Bothitremati- dae, are reassigned to the Gyrodactylidea based, in part, on the common presence of 16 marginal hinged "gyrodactylid" hooks in the haptors of the oncomiracidium and adult.

Our analysis also indicates that Lebedev's (1988) conception of the order Monocotylidea is polyphyletic, since he included the Montchadsky- ellidae within it. The Montchadskyellidae appar- ently had an independent origin within the Po- lyonchoinea, and we therefore propose its removal from the Monocotylidea and elevation of the monotypic Montchadskyellinea to ordinal status.

At higher taxonomic levels, our revision of the Oligonchoinea differs from that of Lebedev (1988) in only two respects. Firstly, the analysis indicates that the superorder Bothriocotylea Lebedev, 1988, is paraphyletic in that the two included or- ders, the Chimaericolidea and Diclybothriidea, have independent origins within the Oligoncho- inca. Therefore, we do not recognise division of the subclass into the Bothriocotylea and Euco- tylea as proposed by Lebedev (1938). Secondly, our analysis shows that the Pterinotrematidae, characterised by several unique autapomorphic features, has its origin within the Microcotylinea

26 W.A. Boeger and D.C. Kritsky

of the Mazocraeidea; as a result, the Pterinotrem- atidea Mamaev & Lebedev, 1977 is unjustified.

Within the Mazocraeidea, we recognise five suborders: the Mazocraeinea, Gastrocotylinea, Discocotylinea, Hexostomatinea and Microcotyli- nea. Our configuration of the Mazocraeinea is the same as that offered by Lebedev (1988) except that our analysis indicates a separate origin for the Hexostomatidae within the Mazocraeidea. Therefore, we propose the new suborder Hexos- tomatinea to accommodate this family.

Similarly, Lebedev (1988) included the Diclido- phoridae, Anchorophoridae, Macrovalvitremati- dae and Anthocotylidae, along with Discocotyli- dae, Diplozoidae and Octomacridae, within the Discocotylinea. Our analysis does not support in- clusion of the former four families in the suborder. We propose the transfer of the Diclidophoridae to the Microcotylinea; and we tentatively consider the Macrovalvitrematidae and Anchorophoridae synonyms of Diclidophoridae based on Mamaev's (1976) phylogenetic hypothesis for the Diclido- phoridae, Our transfer of the Anthocotylidae to the Gastrocotylinea is supported by the presence of an accessory sclerite within the haptoral sucker.

We recognise the Microcotylinea as the termi- nal subordinal taxon within the Mazocraeidea. This configuration does not differ significantly from that proposed by Lebedev (1988), where his Microcotylinea incorporates the same familial taxa we place in the suborder, except for the Dicli- dophoridae and Pterinotrematidae (see above). The Diplasiocotylidae, originally a member of the Microcotylinea s e n s u Mamaev & Lebedev (1979), was apparently inadvertently omitted from Lebed- ev's (1988) classification scheme.

While our classification is easily reconciled with that of Lebedev (1988), such is not the case with the proposals offered by Malmberg (1990). Our hypothesis and classification and, we believe for the most part, those of Lebedev are based on parsimony considerations during respective character and phylogenetic analyses. On the other hand, Malmberg's strict premise of progressive evolution within the monogenoidean haptor obvi- ates agreement between essentially all polarity de- terminations of character-state series. Predictably,

therefore, Malmberg's and our ideas concerning the evolutionary history of the Monogenoidea would be expected to seriously conflict.

Brooks' (1989b) classification of the Cercomeria is strictly bifurcating and possesses features of a "downward system" (see Mayr & Ashlock, 1991) in which taxa are recognised from the highest cate- gory downward. In his system, the taxon contain- ing the "monogenetic flukes" is a sister to the infraclass Cestodaria comprising the cohorts, Gyr- ocotylidea and Cestoidea (= amphilinids+euces- todes). While the present analysis does not contra- dict this classfication of the Cercomeria, the classification proposed herein, which has more "upward" features, does not meet that offered by Brooks. To do so would require proposal of a large number of new taxa at many levels between those of class and family.

Brooks' (1989b) recognised the "monogenetic flukes" to comprise the infraclass Monogenea, the authorship for which was awarded to van Beneden (1858). While no universal "rules" exist governing proposal and use of taxonomic names assigned above family-group taxa, it should be stated that van Beneden (1858) proposed the epithet "Mono- g6n6ses" at the ordinal level. Carus (1863) was the first to utilise "Monogenea" also at the ordinal level and was given credit for this by Yamaguti (1963) in his account of the group. Apparently, Bychowsky (1937) was the first to provide a name, the Monogenoidea, for the group at the level of class, although he gives recognition to van Be- neden (1858) for being the first to recognise these helminths as a group (Bychowsky, 1957).

As far as we are aware, the only criticism of Bychowsky's name is that it possesses the same ending recommended by the International Code of Zoological Nomenclature for superfamilies (Recommendation 29A). However, since the code does not pertain to taxa above the family-groups and not all superfamilies have the ending "oidea", this appears to be an unjustified reason not to use Bychowsky's epithet. Furthermore, the casual elevation of the ordinal epithet "Monogenea" to the level of class by members of the "Round Table" meeting on "Monogenea: problems of sys- tematics, biology and ecology" in Warsaw, Po-

Phylogeny and classification of the Monogenoidea 27

land, during August, 1978 (see Euzet & Prost, 1981) has caused considerable confusion regard- ing "what to do" with the subordinal taxa of the old "Order Monogenea." Some equally casual workers often and unjustifiably consider the sub- orders, Monopisthocotylea and Polyopisthoco- tylea, to be the subordinate class taxa of the "Class Monogenea" as a result of the round tab- le's resolution. Thus, we feel this resolution has resulted in considerable damage to higher level classification of the "monogenetic flukes" and should be rejected, which we have done with ac- ceptance of the Class Monogenoidea Bychowsky, 1937.

Acknowledgements

We wish to acknowledge the following individuals and agencies for allowing access to specimens in their care: M. Beverley-Burton and L.A. Chish- olm, University of Guelph; O.M. Blanco, Museo de La Plata; D.I. Gibson, British Museum (Natu- ral History); D.C. Gomes, Instituto Oswaldo Cruz; S. Hendrix, Gettysburg College; J.-L. Jus- tine, Museum National d'Histoire Naturelle, Paris; S. Kamegai, Meguro Parasitological Mu- seum; G. Kearn, University of East Anglia; R. Lamothe-Argumedo, Museo del Instituto de Biol- ogia; B. Lebedev, Institute of Biology and Pedol- ogy, Vladivostok; J.R. Lichtenfels & P. Pillit, Un- ited States National Museum, USDA, Beltsville; the late C. MaiUard, Universit6 des Sciences et Techniques du Languedoc; M.H. Pritchard, Uni- versity of Nebraska State Museum; D. Thoney, Virginia Institute of Marine Science; T.A. Timo- feeva and A.V. Gusev, Zoological Institute, St. Petersburg; and E. Willassen, Bergen Museum. Mary Beverley-Burton and L. Chisholm allowed us to review a prepublication manuscript of one of their papers; they and Boris Lebedev also pro- vided constructive review of the manuscript. The Conselho Nacional de Desenvolvimento Cien- tiffco e Tecn61ogico (CNPq), Brasil, provided a study grant (20.0115/84) to WAB.

References

Beneden, P.-J. van (1858) M6moire sur les vers intestinaux. M6moire qui a obtenu de l'Institute de France (Acaddmie des Sciences) le grand prix des sciences physiques pour l'ann6e 1853. Extrait du SupplOment aux Comptes Rendus des Sdances de Acadgmie des Sciences, 2, 376 pp.

Beverley-Burton, M., Chisholm, L.A. & Alison, F.R. (In press) The species of Callorhynchicola Brinkmann (Monog- enea: Chimaericolidae) from Callorhinchus spp. (Chimaeri- formes: Callorhinchidae): adult morphology and the larval haptor. Systematic Parasitology, 24, 201--215.

Beverley-Burton, M., Chisholm, L.A. & Last, P. (1991) Two new species of Chirnaericola Brinkmann (Monogenea: Chi- maericolidae) from lqydrolagus spp. (Chimaeriformes: Chi- maeridae) in the Pacific. Systematic Parasitology, 18. 59- 66.

Brooks, D.R. (1989a) A summary of the database pertaining to the phylogeny of the major groups of parasitic platyhel- minths, with a revised classification. Canadian Journal of Zoology, 67, 714-720.

Brooks, D.R. (1989b) The phylogeny of the Cercomeria (Pla- tyhelminthes: Rhabdocoela) and general evolutionary prin- ciples. Journal of Parasitology, 75, 606-616.

Brooks, D.R., O'Grady, R.T. & Glen, D.R. (1985) The phy- logeny of the Cercomeria Brooks, 1982 (Platyhelminthes). Proceedings" of the Helminthological Society of Washington, 52, 1-20.

Bychowsky, B.E. (1937) [Ontogenesis and phylogenetic inter- relationships of parasitic flatworms.] lzvestiya Akademiya Nauk SSSR, Set. Biologiya, 4, 1353-1383. (In Russian: En- glish translation, 1981, Gloucester Point, Virginia: Virginia Institute of Marine Science, Translation Series no. 26).

Bychowsky, B.E. (1957) [Monogenetic trematodes. Their syste- rnatics and phylogeny.] Moscow-Leningrad: Izdatel'stvo Ak- ademiya Nauk SSSR, 509 pp. (In Russian: English transla- tion, 1961. Washington, DC: American Institute of Biological Sciences, 627 pp.

Bychowsky, B.E., Gusev, A.V. & Nagibina, L.F. (1965) [Monogenetic trematodes of the family Tetraonchoididae Bychowsky, 1951.] Trudy Zoolgicheskogo Instimta Akade- miya Nauk SSSR, 35, 140-166, Izdatel'stvo "Nauka", Mos- cow-Leningrad. (In Russian: English translation, 1967, Gloucester Point, Virginia: Virginia Institute of Marine Sci- ence, Translation Series No. 17).

Carus, J.V. (1863) R~iderthiere, Wtirmer, Echinodermen, Coelenteraten und Protozoen. In: Peters, Carus & Ger- staecker (Eds). Handbuch der Zoologie, 2, 422-600.

Combes. C. (1965) Euzetrema knoepffleri n. gen.. n. sp. (Mon- ogenea), parasite interne d'un amphibien endSmique de corse. Annales de Parasitologie Hurnaine et Comparde, 40, 451-457.

Ehlers, U. (1985) Das phylogenetishche System der Plathel- minthes. Stuttgart: Gustav Fischer Verlag, 317 pp.

Euzet, L. & Prost M. (1981) Report of the meeting on "'Mono- genea: Problems of Systematics, Biology and Ecology." Re- view ~f Advances in Parasitology, Warszawa. pp. 1,003- 1,004.

Fuhrmann, O. (1928) Trematoda. Zweite Klasse des Cladus Plathehninthes. In: Ktikenthal, W. & Krunbach, T. (eds),

28 W.A. Boeger and D.C. Kritsky

Handbuch der Zoologie. Berlin & Leipzig: Walter de Gru- yter & Co., 140 pp.

Gerasev, P.I. (1987) [The order Gyrodactylidea Bychowsky, 1937, its possible relationships, origins, composition and position in the system of monogeneans]. In: Gaevskaja, A.V. et al. (Eds) [Parasitology and pathology of marine organisms.] (Abstracts of the IVth All-Union Symposium), pp. 70-72. Kaliningrad: AtlantNIRO (In Russian: English translation provided by author).

Gusev, A.V. (1976) Freshwater Indian Monogenoidea. Prin- ciples of systematics, analysis of the world faunas and their evolution. Indian Journal of Helminthology, 25 & 26, 1- 241.

Gusev, A.V. (1977) [Principles of construction of the system Monogenoidea by B.E. Bychowsky]. Parazitologicheskii Sbornik, 27, 18-26. (In Russian).

Gusev, A.V. (1978a) [Monogenoidea of freshwater fishes. Principles of systematics, analysis of world fauna and its evolution]. Parazitologicheskii Sbornik, 28, 96-198. (In Russian).

Gusev, A.V. (1978b) Some controversial problems in classifi- cation of monogeneans. Folia Parasitologica, 25, 323-331.

Harris, P.D. (1983) The morphology and life-cycle of the ovi- parous OOgyrodactylus farlowellae gen. et sp. nov. (Mono- genea, Gyrodactylidea). Parasitology, 87, 405-420.

Hennig, W. (1966) Phylogenetic systematics. Urbana: Univer- sity of Illinois Press, 263 pp.

Janicki, C. (1921) Grundlinien einer "Cercomer" - Theorie zur Morphologie der Trematoden und Cestoden. Festschrift zur Feier des 60. Geburtstages von Friedrich Zschokke, 30, 22 pp.

Justine, J.-L. (1991) Cladistic study in the Monogenea (Pla- tyhelminthes), based upon a parsimony analysis of spermi- ogenetic and spermatozoal ultrastructural characters. Inter- national Journal for Parasitology, 21,821-838.

Justine, J.-L., Lambert, A. & Mattei, X. (1985) Spermatozoon ultrastructure and phylogenetic relationships in the mono- geneans (Platyhelminthes). International Journal for Parasit- ology, 15, 601-608.

Justine, J.-L. & Mattei, X. (1986) Ultrastructural observations on fertilization in Dionchus remorae (Platyhelminthes, Mon- ogenea, Dionchidae). Acta Zoologica. Stockholm, 67, 97- 101.

Justine, J.-L. & Mattei, X. (1987) Phylogenetic relationships between the families Capsalidae and Dionchidae (Platyhel- minthes, Monogenea, Monopisthocotylea) indicated by the comparative ultrastructural study of spermiogenesis. Zo- ologica Scripta, 16, 111-116.

Justine, J.-L., Mattei, X. & Euzet, L. (1991) Ultrastructure of spermatozoa in two monopistocotylean monogeneans: Encotyllabe sp. (Capsalidae) and Tetraonchoides sp. (Te- traonchoididae). Annales de Parasitologie Humaine et Com- par~e, 66, 173-178.

Kamegai, S. (1971) On some parasites of a coelacanth (Lati- meria chalumnae): a new Monogenea, Dactylodiscus latim- eris n. g., n. sp. (Dactylodiscidae n. faro.) and two larval helminths. Research Bulletin of the Meguro Parasitological Museum, 5, 1-5.

Kearn, G.C. (1963a) The egg, oncomiracidium and larval de- velopment of Entobdella soleae, a monogenean skin parasite of the common sole. Parasitology, 53, 435-447.

Kearn, G.C. (1963b) The oncomiracidium of Capsala martini- eri, a monogenean parasite of the sun fish (Mola mola). Parasitology, 53, 449-453.

Kearn, G.C. & Vasconcelos, M.E. (1979) Preliminary list of monogenean parasites of Portuguese marine fishes, with a note on Enoplocotyle minima Tagliani, 1912. Boletim do lnstituto Nacional de lnvestiga~Oes Pescas, Lisboa, 1, 25-36.

Khotenovsky, I.A. (1985) [Suborder Octomacrinae Khotenov- sky]. Leningrad: Fauna SSSR, 132, 1-263. (In Russian).

Kritsky, D.C. (1970) Studies on the fine structure of the monog- enetic trematode Gyrodactylus eucaliae lkezaki and Hoff- man, 1957. PhD Thesis, University of Illinois, 530 pp.

Kritsky, D.C. (1976) [Observations on the ultrastructure of spermatozoa and spermiogenesis in the monogenean Gyrod- actylus eucaliae Ikezaki et Hoffman, 1957]. Trudy Biolog- o-Pochvennogo lnstituta, Novaja Seriya, 34, 70-74. (In Rus- sian).

Kritsky, D.C. & Boeger, W.A. (1989) The phylogenetic status of the Ancyrocephalidae Bychowsky, 1937 (Monogenea: Dactylogyroidea). Journal of Parasitology, 75, 207-211.

Kritsky, D.C. & Boeger, W.A. (1991) Neotropical Mono- genea. 16. New species of oviparous Gyrodactylidea with proposal of Nothogyrodactylus gen. n. (Oogyrodactylidae). Journal of the Helminthological Society of Washington, 58, 7-15.

Kritsky, D.C. & Kulo, S.-D. (1992) Schilbetrematoides pseudodactylogyrus gen. et sp. n. (Monogenoidea, Dactyl- ogyridae, Ancyrocephalinae) from the gills of Schilbe in- termedius (Siluriformes, Schilbeidae) in Togo, Africa. Jour- nal of the Helminthological Society of Washington, 59, 195- 200.

Lebedev, B.I. (1972) [The taxonomy of monogeneans of suborder Gastrocotylinea]. In: Investigations on the Fauna, Systematics, and Biochemistry of Helminths in the Far East. Proceedings of the Far-East Science Centre, USSR Academy of Sciences, 11, 121-145. (In Russian).

Lebedev, B.I. (1976) [The status of Anthocotylidae in Oligon- choinea]. Trudy Biologo-Pochvennogo lnstituta, Novaja Seriya, 35, 48-51. (In Russian).

Lebedev, B.I. (1987) [Monogeneans, problems in classification and position in the system], Proceedings of the Institute of Biology and Pedology, Far-East Science Centre, USSR Acad- emy of Sciences, 38 pp. (Preprint, in Russian).

Lebedev, B.I. (1988) Monogenea in the light of new evidence and their position among platyhelminths. Angewandte Para- sitologie, 29, 149-167.

Lebedev, B.I. (1989) [On the system of class Monogenoidea]. In: Investigation in Parasitology, Far-East Science Centre, USSR Academy of Sciences, p. 16-23. (In Russian).

Lim, L.H. & Furtado, J.I. (1985) Sundanonchus g. n. (Mono- genea, Tetraonchoididae) from two Malaysian freshwater fishes. Folia Parasitologica, 32, 11-19.

Llewellyn, J. (1963) Larvae and larval development of mono- geneans. Advances in Parasitology, 1,287-326.

Llewellyn, J. (1965) The evolution of parasitic platyhetminths. In: Taylor, A.E.R. (Ed.) Evolution of parasites. Symposia of the British Society for Parasitology, 3, 47-78.

Llewellyn, J. (1968) Larvae and larval development of mono- geneans. Advances in Parasitology, 6, 373-383.

Llewellyn, J. (1970) Monogenea. In: Technical reviews: tax- onomy, genetics and evolution of parasites. Second Interna-

Phylogeny and classification of the Monogenoidea 29

tional Congress of Parasitology. Journal of Parasitology, 56, Sect. II, Pt. 3,493-504.

Lyons, K.M. (1966) The chemical nature and evolutionary significance of monogenean attachment sclerites. Parasit- ology, 56, 63-100.

Maddison, W.P., Donoghue, M.J. & Maddison, D.R. (1984) Outgroup analysis and parsimony. Systematic Zoology, 33, 83-103.

Malmberg, G. (1990) On the ontogeny of the haptor and the evolution of the Monogenea. Systematic Parasitology, 17, 1-65.

Malmberg, G. & Fernholm, B. (1989) Myxinidocotyle gen. n. and Lophocotyle Braun (Platyhelminthes, Monogenea, Acanthocotylidae) with descriptions of three new species from hagfishes (Chordata, Myxinidae). Zoologica Scripta, 18, 187-204.

Mamaev, Yu.L. (1976) [The system and phylogeny of mono- geneans of the family Diclidophoridae]. In: Fauna and syste- matics and phylogenetics of Monogenoidea. Trudy Biolog- o-Pochvennogo Instituta, Novaya Seriya, 35, 57-80. (In Rus- sian).

Mamaev, Yu.L. & Lebedev, B.I. (1977) [System of higher monogeneans in the light of modern data]. In: lssledovanid Monogenej v SSSR, pp. 21-26. (In Russian).

Mamaev, Yu.L. & Lebedev, B.I. (1979) The system of higher monogeneans in the light of recent knowledge. Zoologica Scripta, 8, 13-18.

Mamaev, Yu.L. & Parukhin, A.M. (1981) [A new species of the genus Helixaxine and status of this genus in the system of Monogenea]. Zoologicheskii Zhurnal, 60, 1,455-1,460. (In Russian).

Mamaev, Yu.L. & Slipchenko, N.S. (1975) [Mazoplectus in- eptus gen. et sp. nov. - A representative of a new family of high monogeneans]. In: Parazity i Parazitozy shivotnykh i cheloveka. Kiev: Naukova "Dumka", pp. 171-180. (In Russian).

Mafif-Garz6n, F. & Gil, O. (1962) Trematodos de las tortugas del Uruguay, VI. lagotrema uruguayensis n. gen., n. sp., Monogenea Monopisthocotylea de la vejiga urinaria de Hyd- romedusa tectifera (Cope). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo, 7, 1-7.

Mayr, E. & Ashlock, P.D. (1991) Principles of systematic zoology. New York: McGraw-Hill Inc., 475 pp.

Ogawa, K. & Egusa, S. (1981) The systematic position of the genus Anoplodiscus (Monogenea: Anoplodiscidae). Syste- matic Parasitology, 2,253-260.

O'Grady, R.T. & Deets, G.B. (1987) Coding multistate characters, with special reference to the use of parasites as characters of their hosts. Systematic Zoology, 36, 268-279.

Palombi, A. (1943) Notizie elmintologiche. IV. Anoplodiscus richardi Sonsino e Anoplocotyle australis (Harvey Johnston) nom. nov., loro posizione sistematica. Annuario del Museo Zoologico della Reale Universit?~ di Napoli, 7, 1-3.

Price, E.W, (1936) North American monogenetic trematodes. The George Washington University Bulletin, Summaries" of Doctoral Theses, 1934-36, pp. 10-13.

Price, E.W. (1937a) North American monogenetic trema- todes. I. The superfamily Gyrodactyloidea. Journal of the Washington Academy of Sciences, 27, 114-130.

Price, E.W. (1937b) North American monogenetic trema- todes. I. The superfamily Gyrodactyloidea (continued).

Journal of the Washington Academy of Sciences, 27, 146- 164.

Price, E.W. (1938a) North American monogenetic trema- todes. II. The families Monocotylidae, Microbothriidae, Acanthocotylidae and Udonellidae (Capsaloidea), Journal of the Washington Academy of Sciences, 28, 109-126.

Price, E.W. (1938b) North American monogenetic trema- todes. II. The families Monocotylidae, Microbothriidae, Acanthocotylidae and Udonellidae (Capsaloidea) (con- tinued). Journal of the Washington Academy of Sciences, 28, 183-198.

Price, E.W. (1939a) North American monogenetic trema- todes. III. The family Capsalidae (Capsaloidea). Journal of the Washington Academy of Sciences, 29, 63-92.

Price, E.W. (1939b) North American monogenetic trema- todes. IV. The family Polystomatidae (Polystomatoidea). Proceedings of the Helminthological Society of Washington, 6, 8O-92.

Price E.W. (1942) North American monogenetic trematodes. V. The family Hexabothriidae, n. n. (Polystomatoidea). Proceedings of the Helminthological Society of Washington, 9, 39-56.

Price, E.W. (1943a) North American monogenetic trema- todes. VI. The family Diclidophoridae (Diclidophoroidea). Journal of the Washington Academy of Sciences, 33, 44-54.

Price, E.W. (1943b) North American monogenetic trema- todes. VII. The family Discocotylidae (Diclidophoroidea). Proceedings of the Helminthological Society of Washington, 10, 10-15.

Price, E.W. (1961a) North American monogenetic trema- todes. VIII. The family Hexostomatidae. Proceedings of the Helminthological Society of Washington, 28, 4-9.

Price, E.W. (1961b) North American monogenetic trema- todes. IX. The families Mazocraeidae and Plectanocotyli- dae. Proceedings of the Biological Society of Washington, 74, 127-156.

Price, E.W. (1962a) North American monogenetic trema- todes. X. The family Axinidae, Proceedings of the Hel- minthological Society of Washington, 29, 1-18.

Price, E.W. (1962b) North American monogenetic trema- todes. XI. The family Heteraxinidae. Journal of Parasit- ology, 48, 402-418.

Rohde, K. (1977) Habitat partitioning in Monogenea of mar- ine fishes. Heteromicrocotyla australiensis, sp. nov. and Het- eromicrocotyloides mirabilis, gen. and sp. nov. (Heteromic- rocotylidae) on the gills of Carangoides emburyi (Carangidae) on the Great Barrier Reef, Australia. Zeitsch- rift fiJr Parasitenkunde, 53, 171-182.

Spengel, J.W. (1905) Betrachtungen fiber die Architektonik der Tiere. Zoologische Jahrbiicher, 8, suppl., 639-654.

Sproston N.G. (1946) A synopsis of the monogenetic trema- todes. Transactions of the Zoological Society of London, 25, 185-600.

Timofeeva, T.A. (1988) Position of dionchids in Monogenea. In: Abstracts of Papers, 1st International Symposium on Monogenea, 7-13 August 1988. (~esk6 Bud~jovice: Institute of Parasitology, Czechoslovak Academy of Science, p. 59.

Timofeeva, T.A. & Sharpilo, V.P. (1979) [Euzetrerna caucas- ica sp. n. (Monogenea, Polyopisthocotylidea), a parasite of Mertensiella caucasica]. Parazitologiya, 13, 518-521. (In Russian).

30 W.A. Boeger and D.C. Kritsky

Watrous, L.E. & Wheeler, Q.D. (1981) The outgroup com- parison method of character analysis. Systematic Zoology, 30, 1-11.

Wiley, E.O. (1981) Phylogenetics. The theory and practice of phylogenetic systematics. New York: John Wiley & Sons, 439 pp.

Yamaguti, S. (1963) Systema helrninthum. IV. Monogenea and Aspidocotylea. New York: Interscience Publishers 699 pp.

Yamaguti, S. (1965) New monogenetic trematodes from Hawaiian fishes, I. Pacific Science, 19, 55-95.

Addendum I

Identification of postulated evolutionary changes follow (re- spective homoplasies are listed in parentheses; reversals to symplesiomorphic states are identified by an asterisk): 1 (43), 16 marginal hooks (oncomiracidium); 2 (44), 16 marginal hooks (adult); 3, anchor present; 4, one pair of ventral an- chors; 5 (155), eyes present (oncomiracidium); 6, 2 pairs of eyes (adult); 7, mouth ventral; 8, sperm microtubules lying along 1/4 of cell periphery; 9, male copulatory organ scler- otised; I0 (105, 131, 140, 174), male copulatory organ muscu- lar, elongate; 11 (133, 143, 154), spines of male copulatory organ absent; 12, 14 marginal, 2 central hooks (oncomiracid- ium); 13, 14 marginal, 2 central hooks (adult); 14, 2 sperm axonemes, 1 reduced; 15 (30, 93), 14 marginal hooks (oncomir- acidium); 16 (31, 38, 94), 14 marginal hooks (adult); 17 (37, 60), germarium/oviduct looping right caecum; 18 (29, 40), egg tetrahedral; 19 (104), oral sucker absent; 20, sperm microtub- ules absent; 21 (134), single genital aperture marginal; 22 (45), hook hinged; 23 (53, 146, 166), anchor absent in all developmental stages; 24 (49, 66, 85, 96, 110, 167), eyes absent (oncomiracidium); 25 (83), caeca confluent; 26, testes double; 27* (46), male copulatory organ muscular; 28 (106, 125, 172), sac of male copulatory organ present; 29 (18, 40), egg tetrahed- ral; 30 (15, 93), 14 marginal hooks (oncomiracidium); 31 (16, 38, 94), 14 marginal hooks (adult); 32 (39), one midventral "true" vagina; 33, vas deferens looping left caecum; 34, access- ory piece present; 35*, mouth subterminal; 36 (51, 91), gut diverticula present; 37 (17, 60), germarium/oviduct looping right caecum; 38 (16, 31, 94), 14 marginal hooks (adult); 39 (32), one midventral "true" vagina; 40 (18, 29), egg tetrahed- ral; 41, one ventral bar; 42, 2 ventral bars; 43 (1), 16 marginal hooks (oncomiracidium); 44 (2), 16 marginal hooks (adult); 45 (22), hook hinged; 46* (27), male copulatory organ muscu- lar; 47* (67), egg oval; 48, vagina absent; 49 (24, 66, 85, 96, 110, 167), eyes absent (oncomiracidium); 50 (69, 150), gut single; 51 (36, 91), gut diverticula present; 52 (108), hooks absent (adult); 53 (23, 146, 166), anchor absent in all develop- mental stages; 54, 2 pairs of eyes, posterior pair fused (adult); 55 (57), sperm with one axoneme; 56, 2 pairs of ventral an- chors; 57 (55), sperm with one axoneme; 58 (72), 12 marginal, 2 central hooks (oncomiracidium); 59, 12 marginal, 2 central hooks (adult); 60 (17, 37), germarium/oviduct looping right caecum; 61, 10 marginal, 2 central, 4 dorsal hooks (adult); 62, haptor dactylogyrid; 63", bars absent; 64, 2 lateral "true" vaginae; 65, 2 pairs of anchors, one dorsal, one ventral; 66 (24, 49, 85, 96, 110, 167), eyes absent (oncomiracidium); 67*

(47), egg oval; 68, one ventral, one dorsal bar; 69 (50, 150), gut single; 70 (75), one ventral, 2 dorsal bars; 71, 2 pairs of eyes, posterior pair fused (oncomiracidium); 72 (58), 12 marginal, 2 central hooks (oncomiracidium); 73, 8 marginal, 2 central, 4 dorsal hooks (adult); 74", pathway of germari- urn/oviduct intercaecal; 75 (70), one ventral, 2 dorsal bars; 76, more than 2 testes; 77, gastro-intestinal canal present; 78, haptoral suckers present (adult); 79, hook associated with hap- toral sucker (adult); 80, 3 pairs of haptoral suckers; 81, 2 lateral "ductus vaginalis"; 82 (107, 147), egg filaments absent; 83 (25), caeca confluent; 84, one pair of haptoral suckers; 85 (24, 49, 66, 96, 110, 167), eyes absent (oncomiracidium); 86 (171), "crochet en fl6au" hook-like; 87, "crochet en fl6au" present; 88, one pair of lateral sclerites; 89, lateral sclerites present; 90, 4 pairs of haptoral suckers; 91 (36, 51), gut di- verticula present; 92, mid-sclerite terminates in hook; 93 (15, 30), 14 marginal hooks (oncomiracidium); 94 (16, 31, 38), 14 marginal hooks (adult); 95, germarium lobate; 96 (24, 49, 66, 85, 110, 167), eyes absent (oncomiracidium); 97, 2 ventral hooks (adult); 98, hook associated with haptoral sucker only during larval stage(s); 99 (122), germarium elongate U-shaped; 100, 10 marginal hooks (oncomiracidium); 101, haptoral suck- ers present in appendix; 102", lateral sclerites absent; 103 (7), mouth ventral; 104 (19), oral sucker absent; 105 (10, 131,140, 174), male copulatory organ muscular, elongate; 106 (28, 125, 172), sac of male copulatory organ present; 107 (82, 147), egg filaments absent; 108 (52), hooks absent (adult); 109", "crochet en fl6au" absent; 110 (24, 49, 66, 85, 96, 167), eyes absent (oncomiracidium); 111, 2 oral suckers present; 112, germarium elongate, inverted U-shaped; 113, egg with 2 fila- ments; 114, mid-sclerite flared or truncate; 115, one pair of eyes fused (oncomiracidium); 116, eyes absent (adult); 117, 2 pairs of lateral sclerites; 118, posterior mid-sclerite plate-like; 119 (152, 165), 2 pairs of lateral sclerites, posterior pair broken; 120, "crochet en fl6au" plectanocotylid; 121, 2 pairs of lateral sclerites, anterior pair distally fused, distal posterior pair fused; 122 (99), germarium elongate, U-shaped; 123, "crochet en fl~au" microcotylid; 124, accessory sclerite parallel to mid-sclerite; 125 (28, 106, 172), sac of male copulatory organ present; 126, accessory sclerite perpendicular to mid- sclerite; 127, "crochet en fl6au" gastrocotylid; 128, testis(es) anterior to germarium; 129, one ventro-lateral "ductus vagina- lis"; 130" (142), sac of male copulatory organ absent; 131 (10, 105, 140, 174), male copulatory organ muscular, elongate; 132 (139), "crochet en fl6au" absent (adult); 133 (11, 143, 154), spines of male copulatory organ absent; 134 (21), single genital aperture marginal; 135 (137), haptoral suckers numerous, gas- trocotylid; 136, one mid-ventral "ductus vaginalis"; 137 (135), haptoral suckers numerous, gastrocotylid; 138 (153), one mid- dorsal "ductus vaginalis"; 139 (132), "crochet en fl6au" absent (adult); 140 (10, 105,131,174), male copulatory organ muscu- lar, elongate; 141 (161), 2 dorsal "ductus vaginalis"; 142" (130), sac of male copulatory organ absent; 143 (11,133,154), spines of male copulatory organ absent; 144, haptoral suckers present (oncomiracidium); 145, 6 marginal hooks (oncomiraci- dium); 146 (23, 53, 166), anchor absent in all developmental stages; 147 (82, 107), egg filaments absent; 148", single testis; 149, 4 marginal hooks (oncomiracidium); 150 (50, 69), gut single; 151" (169), egg with one filament; 152 (119, 165), 2 pairs of lateral sclerites, posterior pair broken; 153 (138), one mid-dorsal "ductus vaginalis"; 154 (11, 133, 143), spines of

P h y l o g e n y and c lass i f ica t ion o f t he M o n o g e n o i d e a 31

male copulatory organ absent; 155 (5), 2 pairs of eyes (oncomi- racidium); 156, germarium elongate, double inverted U- shaped; 157, bilateral, armed muscular pads of genital atrium present; 158 (175), genital atrium armed; 159, 2 pairs of eyes, anterior pair fused (oncomiracidium); 160, numerous haptoral suckers, microcotylid; 161 (141), 2 dorsal "ductus vaginalis"; 162", bilateral, armed muscular pads of genital atrium absent; 163, posterior mid-sclerite rod-shaped; 164, numerous haptor- al suckers, diclidophorid; 165 (119, 152), 2 pairs of lateral sclerites, posterior pair broken; 166 (23, 53, 146), anchor ab- sent in all developmental stages; 167 (24, 49, 66, 85, 96, 110), eyes absent (oncomiracidium); 168, fire-tong sucker present; 169" (151), egg with one filament; 170, 2 ventral hooks, 4 hooks in each of 2 lappets (adult); 171" (86), "crochet en flrau" hook-like; 172 (28, 106, 125), sac of male copulatory organ present; 173, haptoral suckers numerous, fire tong; 174 (10, 105,131,140), male copulatory organ muscular, elongate: 175 (158), genital atrium armed.

A d d e n d u m II

In the following list of specimens studied, acronyms are BM (Bergen Museum, Bergen, Norway); BM(NH) (British Mu- seum [Natural History[, London); HWML (University of Neb- raska State Museum, Lincoln, Nebraska); INPA (Instituto Na- cional de Pesquisas da Amazrnia, Manaus, Amazonas, Brazil); IOC (Instituto Oswaldo Cruz, Rio de Janeiro, Brazil); MIBM (Museo del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Mexico City, Mexico); MNHN (Mu- seum National d'Histoire Naturelle, Paris, France); MP (Museo de La Plata, La Plata, Argentina); MPM (Meguro Parasitological Museum, Tokyo, Japan); USNM (United States National Museum, USDA, Beltsville, Maryland); VIMS (Virginia Institute of Marine Science, Gloucester Point, Vir- ginia); and ZIAC (Zoological Institute of the USSR Academy of Sciences, Leningrad). Specimens from the private collec- tions of M. Beverley-Burton & L. Chisholm (MBB-LC), Guelph, Ontario, Canada; the late C. Maillard (CM), Montpellier, France; G. Kearn (GK), Norwich, UK; B.I. Le- bedev (BL), Vladivostock, Russia; and Sherman Hendrix (SH), Gettysburg, Pennsylvania, USA, were also used.

Monoeotylidae: Voucher, Monocotyle diademalis, HWML 1454; 2 vouchers, M. dasybatis, HWML 1557; paratype, M. kuhlii, USNM 61743; 2 paratypes, M. granulatae, USNM 61741; 2 paratypes, M. tritestis, USNM 61745; 3 vouchers, Merizocotyle dasybatis, USNM 35163. Loimoidae: 22 cotypes, Loimos salpingoides, USNM 35675; 3 paratypes, L. scoli- odoni, HWML 20494. Acanthocotylidae: 2 vouchers, Acantho- cotyle Iobianchi, GK; 2 paratypes, A. pugetensis, USNM 9198; 3 paratypes, A. pacifica, USNM 9200; holotype, paratype, Enoplocotyle hawaiensis, USNM 63603. Capsalidae: Voucher, Capsala molae, USNM 42594; 3 vouchers, C. martinieri, HWML 1453; voucher, C. pricei, HWML 1421:3 vouchers, C. laevis, HWML 22412, 22413; voucher, C. poeyi, HWML 22414; voucher, C. ovalis, HWML 23292. Dionehidae: 4 vouch- ers, Dionchus agassizi, USNM 3577, 35678; 16 vouchers, D. remorae, USNM 35681, 35682, 35683. Montehadskyellidae: 3 paratypes, Montchadskyella intestinale, ZIAC 3678, 3679,

3680. Gyrodaetylidae: 9 paratypes, Ooegyrodactylus farlowel- lae, USNM 77095, BM(NH) 1982.3.30.1-9; holotype, 9 para- types, Phanerothecium caballeroi, USNM 73407, 73408, 73409, 73410; holotype, P. harrisi, INPA PA 333; holotype, Notho- gyrodactylus clavatus, INPA PA330; holotype, N. amazonicus, INPA PA 331; holotype, N. plaesiophallus, INPA PA 332. Bothitrematidae: 6 cotypes, 7 vouchers, Bothitrema bothi, USNM, 35186, 35706, SH; 2 vouchers, B. sp., ZIAC (no number). Tetraonchoididae: 2 vouchers, Tetraonchoides para- doxus, ZIAC 5395, 5396; voucher, T. japonicus, ZIAC 3465; 4 vouchers, Pavlovskioides littoralis, ZIAC 3330, 3331, 3322; 2 vouchers. 3 homeotypes, P. antarcticus, ZIAC 41,42, USNM 62881; 2 paratypes, P. trematomi, USNM 62883; 3 paratypes, P. wilkesensis, USNM 62885; 2 paratypes, Allotetraonchoides rhigophilae, USNM 62887. Calceostomatidae: 2 vouchers, Cal- ceostomella inermis, ZIAC 10339, 10340; paratype, Calceo- stoma herculanae, MNHN Tj 204; paratype, Paracalceostoma sciaenae, MPM 17385. Neodactylodiseidae: 3 paratypes, Neo- dactylodiscus latimeris, MPM 16698. Amphibdeilatidae: 3 para- types, Amphibdella cuticulovagina, USNM 61066; 10 cotypes, A. fluvolineatus, USNM 35159; holotype, 6 paratypes, Am- phibdelloides rnaccaUumi, USNM 35700; homeotype, A. mc~c- callumi, USNM 61067; voucher, A. maccallumi, USNM 49039. Tetraonchidae: 2 paratypes, Tetraonchus alaskensis, USNM 41141; 3 vouchers, T. monenteron, USNM 38482. Neotetraon- chidae: Holotype, voucher, Neotetraonchus bychowskyi, MIBM 223-8, USNM 80467. Daetylogyridae: 3 paratypes, An- cylodiscoides caecus, USNM 70995, 73566; holotype, 5 para- types, 2 vouchers, A. parasiluri, MPM 22591, ZIAC 35734; holotype, 2 paratypes, A. hamatovagina, MPM 22598; 4 para- types, 2 vouchers, A. asoti, MPM 22593, ZIAC (no number); holotype, A. sigmoidovagina, MPM 22595:2 paratypes, A. infundibulovagina, MPM 22596; holotype, paratype, A. gigi, MPM 22597:4 vouchers, Pseudodactylogyrus anguillae, MPM 19140:2 vouchers, P. bini, MPM 19140; holotype, voucher, P. microrchis, MPM 19139, 19140; holotype, 6 paratypes, 5 vouchers, P. apogonis, MPM 22339, 19414; 2 paratypes, Hare- ocephalus thaisae, USNM 60878; 2 vouchers, Linguadaco, lo- ides brinkmanni, USNM 80431; 2 vouchers, Heterotesia voltae, USNM 80430. Diplectanidae: 7 vouchers, Diplectanum hilum, USNM 80427; 2 vouchers, D. piscinarius, USNM 80428; voucher, D. pescadae, USNM 80429. Pseudumurraytremati- dae: 2 vouchers, Pseudomurraytrema copulatum, USNM 73573; 3 vouchers, P. paradoxum, USNM 73575; 3 vouchers, P. etowanum, USNM 73579:3 vouchers, P. rogersi, USNM 74005. Polystomatidae: 2 vouchers, Polystoma sp., USNM 43005; 2 cotypes, P. aspidonectes, USNM 35577: cotype, P. rugosa, USNM 35581; holotype, P. elegans, USNM 35579. Sphyranuridae: 2 vouchers, Sphyranura osleri, HWML 1455, 20278" 8 cotypes, S. eurrceae, USNM 36873. Chimaericolidae: Holotype, paratype, voucher, Callorhynchicola multitesticul- atus, USNM 37445, 37446; 2 vouchers, C. multitesticulatus, MBB-LC; vouchers (2 on slides, many unmounted), Chimaer- icola leptogaster, BM; voucher, C. colliei. MBB-LC. Di- clybothriidae: 7 vouchers. Diclybothrium armature, USNM 73136, 35584, 35287; 19 vouchers, D. hamulatum, HWML 20494. Hexahothriidae: 7 vouchers, Hexabothrium appendicul- atum, USNM 63398, HWML 1408; GK; 5 paratypes, H. mus- teli, USNM 8132; 3 paratypes, H. akaroensis, USNM 71195, VIMS (no number); holotype, 2 paratypes, Dasyonchocoo,le spiniphallus. USNM 38148, VIMS (11o number): holotype, 8

32 W.A. Boeger and D.C. Kritsky

paratypes, D. dasyatis, USNM 63690; 3 homeotypes, Erpoco- tyle antarctica, USNM 71196; holotype, E. ginglymostomae, USNM 8810; 2 neotypes, E. laevis, MNHN 190Ti 147P; 4 paratypes, E. rnaccallumi, USNM 8139; 9 cotypes, E. mac- rohystera, USNM 8138; 3 vouchers, E. sp., USNM 77517; 3 paratypes, E. sphyrnae, USNM 8137; paratype, E. tiburonis, HWML 1420; holotype, 4 paratypes, E. mavori, USNM 8155; holotype, paratype, Rhinobatonchocotyle cyclovaginatus, USNM 47833, USNM 61039; holotype, paratype, Heteroncho- cotyle hypoprioni, USNM 8809, HWML 1417; holotype, 5 paratypes, 2 vouchers, H. leucas, USNM 38149, 61316, 71469, VIMS (no number); 2 paratypes, Paraheteronchocotyle arna- zonensis, HWML 21391; 2 paratypes, Squalonchocotyle cen- trophori, MNHN 710H Ti50, CM; 2 paratypes, vouchers (many unmounted, 4 mounted), S. somniosi, USNM 37458, 50403; 6 paratypes, S. squali, USNM 8134; paratype, 3 vouch- ers, S. impristi, USNM 38150, VIMS (no number); 3 vouchers, Protocotyle grisea, MNHN ll0H Tc45, CM; 8 paratypes, P. taschenbergi, MNHN l l l H Tc48, CM; 12 vouchers, Epicotyle torpedinis, CM, MNHN (no number); holotype, 17 vouchers, Callorhynchocotyle marplatensis, MP P-12, MP 1613 D, USNM 80279, HWML 20705, 20706, IOC 32.442; holotype, paratype, C. callorhynchi, USNM 37447; holotype, 7 para- types, C. amatoi, USNM 37448, 71197, HWML 1442; para- type, Neonchocotyle pastinacae, CM; 3 paratypes, Pseudohex- abothrium rajae, BM 42923. Plectanoeotylidae: Voucher, Plectanocotyle gunardi, HWML 1411. Mazoeraeidae: 2 para- types, Mazocraeoides olentangiensis, USNM 38340; 2 para- types, M. sardinellae, MP Ti83, Ti84; 4 vouchers, Kuhnia scornbri, USNM 35618, 35620. Anthoeotylidae: 7 vouchers, Anthocotyle americanus, USNM 8191, 35607, 35608. Protomic- rocotylidae: 10 cotypes, Protomicrocotyle rnirabile, USNM 35628; 3 vouchers, P. manteri, MIBM 222-24. AIIodiscoeotyli- dae: 2 paratypes, Allodiscocotyla mexicana, MIBM 219-2; holotype, 20 paratypes, A. lae, USNM 63667. Chauhaneidae: 4 vouchers, Chauhanea madrasensis, ZIAC 6474, 6475. Gas- trocntylidae: 2 vouchers, Gastrocotyle trachuri, USNM 63387, 75595; 2 vouchers, Gastrocotyle sp., USNM 63389, 36458. Neothoracoeotylidae: Paratype, 7 vouchers, Neothoracocotyle acanthocybii, USNM 9174, HWML 1426. GotoeotyHdae: Voucher, Gotocotyle bivaginalis, HWML 1406; voucher, G. secunda, HWML 1407; 3 vouchers, Gotocotyle sp., HWML 1687, ZIAC (no number). Pseudodielidophoridae: Holotype,

11 paratypes, Pseudodiclidophora decapteri, USNM 63507. Discocotylidae: 7 vouchers, Discocotyle salmonis, USNM 35171. Diplazoidae: 3 vouchers, Diplozoon nipponicurn, HWML 23293, 23294; 2 paratypes, D. aegyptensis, USNM 59654. Oetomacridae: 2 cotypes, 9 vouchers, Octomacrum lan- ceolatum, USNM, 32570, 20498, HWML 20499, 20498; 2 para- types, O. semotili, USNM 61683. Hexnstomatidae: Holotype, voucher, Hexostoma macracanthum, USNM 36890, HWML 21451; holotype, H. lintoni, USNM 6676. Axinidae: Holotype, Axine resplendens, MIBM 25-24; paratype, A. yamagutii, HWML 1445; 3 vouchers, A. belones, USNM 37726, 37727. Diplasiocotylidae: 2 homeotypes, Diplasiocotyle johnstoni, USNM 61090. Heteraxinidae: Paratype, Heteraxine seriola, USNM 37729; 2 paratypes, Allencotyle mcinthoshi, USNM 37731; holotype, paratype, Cemocotyle trachuri, USNM 61087; voucher, C. noveborencis, MIBM 220-13; 2 paratypes, C. saqae, HWML 1544; 28 vouchers, C. carangis, USNM 37737, 37736, 37735. Microcotylidae: 2 vouchers, Microcotyle poma- tomi, USNM 35319; voucher, M. macroura, USNM 35146; 2 vouchers, M. pomacanthi, USNM 35134; 7 vouchers, M. sebastis, USNM 80467. Allopyragraphoridae: Paratype, Allop- yragraphorus caballeroi, MIBM 216-22; 3 vouchers, A. incom- parabilis, USNM; holotype, 4 paratypes, Allomicrocotyla onaga, USNM 63517. Diclidophoridae: Voucher, Diclidophora palmata, GK; voucher, D. luscae, GK; voucher, 2 paratypes, D. rnerlangi, GK, HWML 21365; 2 vouchers, D. embiotocae, HWML 23524, USNM 79494; voucher, D. maccallurni, USNM 35585; voucher, Diclidophora sp., USNM 63396; paratype, Macrovalvitrema sinaloense, MIBM 213-5; paratype, Pterino- trematoides mexicanum, MIBM 213-6; holotype, 2 paratypes, Papillopseudotagia hubbsi, USNM 79500, 79501, HWML 23690; holotype, paratype, Pseudohargisia cortesi, USNM 79499, HWML 23641; 2 vouchers, Anchorophorus sinensis, ZIAC 6186, 6188. Pterinotrematidae: 2 paratypes, Pterino- trema macrostomum, MIBM 212-24, 220-16; 2 paratypes, P. mirabilis ZIAC 6140, 6141; holotype, 7 paratypes, Pseudopter- inotrema albulae, USNM 63548. Pyragraphoridae: Voucher, Pyragraphorus pyragraphorus, HWML 1413; paratype, P. hol- lisae, MNHN T 170. Heteromicrocotylidae: 2 vouchers, Hetero- microcotyle sp., ZIAC 10236; voucher, Heterapta sp., USNM 80466; 5 vouchers, H. polyorchis, BL 2407. Mierobothriidae: 12 cotypes, Microbothrium apiculatum, USNM 35684, 35685, 35686.