Phylogeny and a revised classification of the Monogenoidea ...

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

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Phylogeny and a revised classification of the Monogenoidea Bychowsky, 1937 (Platyheiminthes) Walter A. Boeger ~ and Delane C. Kritsky2 ~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 Monogenoidea 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 Oligonchoinca, 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 Neodactylodiscinea and Amphibdellatinea are proposed to reflect these origins. The Gyrodactylidea (Polyonchoinca) is supported by three synapomorphies and comprises the Gyrodactylidae, Anoplodiscidae, Tetraonchoididae and Bothitrematidae. The analysis supports recognition of the Polystomatoinea comprising Polystomatidae and Sphyranuridae. Evolutionary relationships within the Oligonchoinea indicate independent origins of three ordinal taxa, the Chimaericolidea (monotypic), Diclybothriidea (including Diclybothriidae and Hexabothriidae) and Mazocraeidea (with five suborders). The suborder Mazocraeinea comprises the Plectanocotylidae, Mazocraeidae and Mazoplectidae, and is characterised by two synapomorphies. The suborder Gastrocotylinea, characterised by presence of accessory sclerites in the haptoral sucker, is divided into two infraorders, the monotypic Anthocotylina infraorder novum and Gastrocotylina. Two superfamilies of the Gastrocotylina are recognised, the Protomicrocotyloidea and Gastrocotyloidea; 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, Gotocotyloidea, Anchorophoridae and Macrovalvitrematidae. The Sundanonchidae, Iagotrematidae and Microbothriidae were not included in the analysis because of lack of pertinent information regarding character states.

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W.A. Boeger and D.C. Kritsky

Introduction

The phylogenetic relationships of the Monogenoidea* have been controversial since Bychowsky (1937, 1957) revived Spengel's (1905) notion of consanguinity of the cestodes and monogenoideans. Bychowsky's phylogenetic hypothesis and classification for the Monogenoidea, based primarily on larval characters, differed from the then contemporary and established system of Fuhrmann (1928), who promoted sister relationship of the digeneans and monogeneans as proposed by Janicki (1921). Bychowsky's system has been frequently revised to accommodate new discoveries (e.g. Gusev, 1976, 1977, 1978a,b; Lebedev, 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 hypothesis for the Monogenoidea utilising larval and some post-larval features primarily of the haptor. LleweUyn did not provide a congruent classification, but his analysis suggested additional evolutionary avenues within the class. Malmberg (1990) proposed a classification based on haptoral structures and on the premise that evolution is progressive, i.e. structures are added as evolution proceeds. Apparently an outcome of his evolutionary 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 ultrastructural information on sperm and spermiogenesis. 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 * U s e of the appelation 'Monogenoidea' rather than the more commonly used ' M o n o g e n e a ' 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 revised classification of the class grounded on the new phylogenetic hypothesis is provided.

Materials and methods

Character states for each familial taxon were initially defined from the literature. Published accounts were verified, when possible, by subsequent 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 information 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 phylogeny. An initial hypothesis on evolutionary relationships of the families of Monogenoidea was constructed using Hennigian Argumentation (Hennig, 1966; Wiley, 1981); the topology of the cladogram was then subjected to PAUP (Phylogenetic Analysis Using Parsimony, Version 2.4.1; D. L. Swofford, Illinois Natural History Survey, Champaign) to confirm that it was a most-parsimonious tree. A total of 141 character states comprising 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). Functional outgroups were used when character states of a transformation series were entirely within the ingroup (Watrous & Wheeler, 1981). The Udonellidea, Trematoda, Gyrocotylidea and Cestoidea were chosen is outgroups based on the phylogenetic 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 respective Articles 23 and 36 of the 1985 International Code of Zoological Nomenclature (ICZN)

Phylogeny and classification of the Monogenoidea 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 Monogenoidea Bychowsky, 1937, since it was the first proposed for the group at the rank of class (see 'Discussion' and Lebedev, 1988).

Results

(010)

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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 evolutionary changes depicted in the cladogram. A list of character state changes with homoplasies is provided in Addendum I; the data matrix is available on computer disc through the University of Nebraska 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 oncomiracidium). Plesiomorphy: (00) two pairs [6]. Apomorphies: (01) two pairs, posterior pair fused [54]; (10) eyes absent [116]. Derived states evolved independently (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

Fig. 1. Hypothesised transformation of character states of the eyes in the oncomiracidium (diagrammatic). Broken arrows represent potential transformations not thought to have occurred 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 constraint. 3. Position of mouth. Plesiomorphy: (0) subtermihal [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 independently (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 single 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 between the Polyonchoinea and Oligonchoinea. 6. Caeca. Plesiomorphy: (0) nonconfluent. Apomorphy: (1) confluent [25, 83]. Initially we considered confluence of simple caeca as the same

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state as anastomoses of intestinal diverticula. Early phylogenetic analyses indicated that anastomoses of diverticula and confluent intestinal caeca correspond to independent evolutionary events. Thus, the character states in this transformation series apply only to taxa primitively lacking 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 Pseudomurraytrematidae contain species with both confluent and nonconfluent 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 polyonchoinean and polystomatoinean families with the plesiomorphic state have species with gut diverticula. The development of diverticula in these families (e.g. Capasalidae, Monocotylidae, Polystomatidae) apparently represents secondary evolutionary phenomena. 8. Testes. Plesiomorphy: (00) single [148]. Apomorphies: (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) posterior 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 axonemes. 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) postulated that the plesiomorphic state for monogenoideans is presence of a sclerotised copulatory organ and consider it homologous to the "cop-

ulatory stylet" of dalyelloids, udonellids and temnocephalids. Comparative morphology of the stylet of dalyelloids does not support this homology. Further, udonellids do not possess a sclerotised 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. Although the state in some temnocephalids is similar to that of most polyonchoineans, optimization of the transformation series (including states in temnocephalids, dalyelloids and udonellids) supports the present polarisation. Another potentially useful feature for phylogenetic 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 analysis by the morphological characters we use, a homologous 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. Plesiomorphy: (0) ovate. Apomorphy: (1) elongate [10, 105, 131, 140, 174]. 16. Spines of male copulatory organ (copulatory organ muscular). Plesiomorphy: (0) present. Apomorphy: (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 female 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 sky, 1985). The Gyrodactylidae and Diplozoidae receive a (9) in the matrix; respective states are autapomorphies that do not contribute evolutionary information regarding the ingroup. 19. Genital atrium. Plesiomorphy: (0) unarmed. Apomorphy: (1) armed [158, 175]. 20. Bilateral, armed muscular pads of genital atrium. Plesiomorphy: (0) absent [162]. Apomorphy: (1) present [157]. 21. Germarium. Plesiomorphy: (00) ovate. Apomorphies. (01) lobate [95]; (10) elongate, Ushaped [99, 122]; (20) elongate, inverted Ushaped [112]; (30) elongate, double inverted Ushaped [156]. See Fig. 2 for ordering (coded by mixed coding). 22. Pathway of germarium/oviduct. Plesiomorphy: (0) intercaecal [74]. Apomorphy: (1) looping right caecum [17, 37, 60]. Our analysis indicates that the looping of the germarium/oviduct around the right caecum represents convergent states in several clades in the Polyonchoinea. The germarial loop is plesiomorphic for the four terminal suborders of the Dactylogyridea (Dactylogyrinea, Tetraonchinea, Amphibdellatinea, Neodactylodiscinea) supporting the polarisation offered by Kritsky & Boeger (1989) for the Dactylogyridae. 23. Genito-intestinal canal. Plesiomorphy: (0) absent (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 plesiomorphic 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 ventrolateral "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 ventro-lateral "ductus vaginalis" [129]; (101010) one mid-ventral "ductus vaginalis" [136]; (000001) va-

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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 vaginalis") 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 ventro-lateral "true" vagina, is plesiomorphic for the ingroup. 25. Egg. Plesiomorphy: (0) oval [47, 67]. Apomorphy: (1) tetrahedral [18, 29, 40]. 26. Egg filaments. Plesiomorphy: (00) one filament [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 bearing") 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. Polarisation suggested by outgroup comparison (plesiomorphy = 10 marginal hooks) was initially considered 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


(oo)

(Ol)

2 Fig. 2. Proposedtransformationof types of germaria in the Monogenoidea(diagrammatic).Numbersin parenthesesindicate the respective code each state receivedin the matrix (homologousseries 21).

equal probability of being lost. Consequently, the 14 hook states of the Calceostomatidae and Dactylogyridae (12 marginal, 2 central) are not homologous 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 Calceostomatidae 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 bearing") 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 marginal, 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 ,

I i

g

,0

0

//-OV

A 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 absent" and "14 marginal hooks" were appropriately 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 gyrodactylid hook based on presence of a "hinge" between the hooklet and shank. The present analysis indicates that the hinged articulation developed 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. Consequently, 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, ventral [56]; (2) two pairs, one ventral, one dorsal [65]. Polarisation is by functional outgroup comparison. 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

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VAGINA ABSENT

(00007

0100)

ONE VENTROLATERAL "TRUE" VAGINA (oooooo)

1

TWO LATERAL "DUCTUS VAGINALIS"

(100000)

ONE VENTROLATERAL "DUCTUS VAGINALIS" (100010)

ONE MIDVENTRAL "DUCTUS VAGINALIS" ,10,010,

ONE MIDDORSAL "DUCTUS VAGINALIS" (200000) l

TWO DORSAL "DUCTUS VAGINALIS" 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 haptoral suckers of most (but not all) of the Mazocraeidea 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. Plesiomorphy: (0) absent. Apomorphy: (1) present [144]. The series is polarised by functional outgroup comparison. 36. Fire-tong sucker (haptoral suckers present). Plesiomorphy: (0) absent. Apomorphy: (1) present (Fig. 8L,M) [168]. Polarisation is by functional outgroup comparison. 37. Association of hook and haptoral sucker (haptoral suckers present). Plesiomorphy: (0) present in adult [79]. Apomorphy: (1) present during development 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" haptoral suckers were considered a single state. Resulting 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 information on sucker type and number. 39. Haptoral suckers in appendix (suckers present). Plesiomorphy: (0) suckers absent. Apomorphy: (1) suckers present [101]. Polarisation of the series is by functional outgroup comparison. 40. Mid-sclerite of sucker (suckers present). Plesiomorphy: (0) absent. Apomorphies: (1) terminates in hook [92]; (2) flared or truncate [114]. Polarisation is by functional outgroup comparison. 41. Posterior mid-sclerite (suckers present). Plesi-


9

(ooo)A

(ioo)

(010)

(2oo)

(020)

(030)

5 Fig. 5. Postulatedtransformationof number and distributionof hooks in the oncomiracidiumof 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 parenthesesindicate the respectivecode each state receivedin the matrix (homologousseries 28).

omorphic: (00) absent. Apomorphies: (10) rodshaped (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 outgroup comparison. 42. Accessory sclerite (suckers present). Plesiomorphy: (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). Plesiomorphy: (0) absent [102]. Apomorphy: (1) present [89]. Polarisation is by functional outgroup comparison.

44. Number of lateral sclerites (when present). Plesiomorphy: (0) one pair [88]. Apomorphies: (1) two pairs (Fig. 8 A - 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). Plesiomorphy: (0) absent [109]. Apomorphy: (1) present [87]. The series is polarised by functional outgroup comparison. Llewellyn (1963) considers the "crochet en fl6au" homologous with hooks (Fig. 6 in Llewellyn, 1963), while other workers (Gusev, 1978b,

10


:Sh (ioooo> C

(10001)

,00 , , , ,

(02000)

.0000\

(99919)

(50000)

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 sclerite as a true anchor. Since there is no definitive evidence to resolve the question, we incorporated three hypotheses into independent analyses as follows: (1) "crochet en fl6au" was considered homologous 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 n o v o " structure while recognising that unequivocal evidence for its origin is lacking.


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

In the present analysis, the existing term "crochet 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 Monogenoidea. 46. "Crochet en fldau" in adult (present in oncomiracidium). Plesiomorphy: (0) present. Apomorphy: (1) absent [132, 139]. Polarisation is by functional outgroup comparison. 47. Shape of "crochet en fl(au" (present in oncomiracidium 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 l D ) [127]. Polarisation is by functional outgroup comparison (coded by mixed coding). Phylogeny and revised classification of the Monogenoidea 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

11

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. Although not used in the analysis, the presence of three rows of ciliary epidermal bands in the oncomiracidium 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 dealing with large terminal taxa such as the Monogenoidea. Therefore, while the present analysis could potentially be used to support other systems, our proposed classification including division of the Monogenoidea into the three subclasses, the Polyonchoinea, Polystomatoinea and Oligonchoinea, as suggested by Lebedev (1988), is based on the hypothesised sequence of appearance of respective taxa within the class: it appears to be a reasonably efficient system while furnishing evolutionary information about the group. The Polyonchoinea is supported by seven synapomorphies, 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 haptors, appear the most significant. The sister relationship of the Polystomatoinea and Oligonchoinea 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 Polystomatoinea and Oligonchoinea is supported by one and seven synapomorphies, respectively. The proposed classification for the familial taxa of Monogenoidea and coordinated with our phylogenetic hypothesis follows:

12


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9

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11

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

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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 Bychowsky, 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


15

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