Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm and Observations on the Early Diversification of Apewormst and Vertebrates

View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by UNL | Libraries

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln

Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

8-1-1999

Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm and Observations on the Early Diversification of apewormsT and Vertebrates

Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected]

Scott Lyell Gardner University of Nebraska - Lincoln, [email protected]

Ronald A. Campbell University of Massachusetts - Dartmouth, [email protected]

Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs

Part of the Biodiversity Commons, Evolution Commons, and the Parasitology Commons

Hoberg, Eric P.; Gardner, Scott Lyell; and Campbell, Ronald A., "Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm and Observations on the Early Diversification of apewormsT and Vertebrates" (1999). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 56. https://digitalcommons.unl.edu/parasitologyfacpubs/56

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Systematic Parasitology (1999) 42: 1–12. Copyright 1999, Kluwer Academic Publishers. Used by permission.

Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm, and Observations on the Early Diversification of Tapeworms and Vertebrates*

Eric P. Hoberg1, Scott L. Gardner2 & Ronald A. Campbell3

1Biosystematics and National Parasite Collection Unit, United States Department of Agriculture, Agricultural Research Service, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20715, USA ([email protected]) 2Harold W. Manter Laboratory of Parasitology, W-529 Nebraska Hall, University of Nebraska, Lincoln, Neb. 68588-0514, USA 3Department of Biology, University of Massachusetts-Dartmouth, N. Dartmouth, Massachusetts 02747, USA

Accepted for publication July 9, 1998.

Abstract

Evolutionary relationships of the Eucestoda have received intense but sporadic attention over the past century. Since 1996, the landscape has dramatically changed with respect to our knowledge of the phylogenetic relationships among the tapeworms. The 2nd International Workshop for Tapeworm System- atics (IWTS) held in Lincoln, Nebraska in October of that year provided the catalyst for development of novel hypotheses for inter-and intra-ordinal phylogeny. The working-group structure of the 2nd IWTS and results of phylogenetic studies are briefly introduced in the present manuscript. Higher-level phylog- enies derived from parsimony analysis of independent data bases representing comparative morphology or molecular sequences were largely congruent and supported monophyly for the Eucestoda. The Caryo- phyllidea are basal; difossate forms such as the Pseudophyllidea are primitive; tetrafossates including the Tetraphyllidea, Proteocephalidea, Nippotaeniidea, Tetrabothriidea and Cyclophyllidea are derived; and hypotheses differed in the placement of the Trypanorhyncha and the Diphyllidea. These studies may provide a foundation for resolution of inter-and intra-ordinal relationships for the tapeworms. Additionally, the first comprehensive phylogenetic hypotheses for the Pseudophyllidea, Diphyllidea, Trypanorhyncha, the paraphyletic Tetraphyllidea + Lecanicephalidea, Proteocephalidea and Cyclophyllidea were developed during and subsequent to the 2nd IWTS. The stage is now set for continued and rapid advances in our understanding of the eucestodes. These studies have also served to re-emphasise the rich genealogical diversity of tapeworms and the temporally deep history for their origin. A co-evolutionary history and radiation of eucestodes may involve deep co-speciation with vertebrate host taxa, accompanied by some level of colonisation and extinction, extending into the Palaeozoic, minimally 350-420 million years ago.

Introduction issues related to the Eucestoda Southwell, 1930 has dramatically increased since the late 1980s Interest in the systematics of the tapeworms has es- (see Brooks & McLennan, 1993; Hoberg et al., 1997b; calated over the past decade. The first phylogenetic Hoberg, 1997; Mariaux, 1998). Higher-level relation- study of cestodes, a treatment of the Proteocepha- ships among the orders have been examined only re- lidea Mola, 1928 was published by Brooks (1978) cently for the first time (e.g. Brookset al., 1991; Brooks more than 20 years ago, but the number of papers & McLennan, 1993), whereas most previous studies addressing phylogeny, co-evolution and historical focused on species or generic genealogical diversity. Interest in the systematics and taxonomy of * A report of results of phylogenetic analyses conducted during tapeworms led to the 1st International Work- the 2nd International Workshop for Tapeworm Systematics, Lin- shop for Tapeworm Systematics (IWTS) chaired coln, Nebraska, October 2-6, 1996; E.P. Hoberg, S.L. Gardner and R.A. Campbell, organizers. Contributions edited by E.P. Hoberg.

1 2 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12. by Claude Vaucher and Jean Mariaux in Ge- of order (chair: E.P. Hoberg); (2) molecular sys- neva, Switzerland in 1993 (Mariaux & Vaucher, tematics (J. Mariaux); (3) ultrastructural characters 1994). At this seminal meeting the conceptual of spermatozoa and spermiogenesis (J.-L. Justine); roots were created to build a broad and coopera- (4) Pseudophyllidea Carus, 1863 (R.A. Bray); (5) tive international research program addressing Tetraphyllidea Carus, 1863, Trypanorhyncha Dies- significant questions in eucestode systematics. ing, 1863 and associated orders (R.A. Campbell); Evolutionary relationships of the eucestodes have (6) Proteocephalidea (A. Rego); and (7) Cyclophyl- received intense but sporadic attention over the past lidea van Beneden in Braun, 1900 (A. Jones). Ad- century, but there has never been a general consen- ditional groups focused on relationships of genera sus among the various hypotheses (see Brooks et al., within families (e.g. Hymenolepididae Ariola, 1899, 1991; Mariaux, 1996; Hoberg et al., 1997b). Conflict- Anoplocephalidae Cholodkowsky, 1902, Metadile- ing opinions over the adequacy of different classes pididae Spasskii, 1959, Paruterinidae Fuhrmann, of morphological and molecular characters as in- 1907) and species within genera (e.g. Taeniidae dicators of relationship, the application of differ- Ludwig, 1886 and species of Taenia Linnaeus, 1758). ent methodologies for phylogenetic reconstruction, Each Working Team produced a summary of and untested assumptions of host-parasite co-spe- characters representing putative homologies for ciation (e.g. the concept that the phylogeny of hosts morphological attributes (including those from mirrors that of the parasite taxon) have contributed light and electron microscopy), ontogeny, or mo- to the current situation (Mariaux, 1996). Although lecular sequence data. Putative transformation se- the most recent diagnostic keys provided compre- ries generated from character descriptions were hensive coverage to the generic level, there was no polarised relative to taxonomic outgroup(s) (Mad- general attempt to reflect evolutionary relation- dison et al., 1984) and summarised in numerical ships (Khalil et al., 1994). Assessments of phyloge- character matrices. These constituted the basis netic diversity, however, have become increasingly for development of phylogenetic hypotheses for important with the advent of biodiversity surveys each taxon under study. Parsimony analyses were and inventories in conservation biology, analyses of conducted with PAUP 3.1.1 and MacClade 3.05 host-parasite co-speciation and historical biogeog- (Swofford, 1993; Maddison & Maddison, 1992). raphy, and strategic research involving agricultur- Phylogenetic hypotheses resulting from these ally and medically important taxa (Hoberg, 1997). analyses represented the first concerted effort to These issues formed the foundation for the 2nd develop a comprehensive knowledge of relation- IWTS held in Lincoln, Nebraska in 1996 (Hoberg et ships for the Eucestoda. In this context, hierarchical al., 1997a). The Workshop was convened to explore and top-down analyses initially addressed higher new and concrete ideas for future progress in tape- level relationships and were in many cases used worm systematics and to work toward standardis- to identify outgroups for sequential and more in- ing research programmes at the international level clusive levels of study within orders. In contrast, with emphasis on phylogenetic systematic analy- bottom-up analyses focused on lower taxonomic sis (Hennig, 1966; Wiley 1981; Wiley et al., 1991). levels and sampled representative genera and spe- Results of the Workshop are now summarised in cies to estimate phylogenetic structure within and part and presented herein as a series of papers ad- among ordinal-level groups. Thus, an array of dressing various aspects of eucestode phylogeny. characters with different levels of universality (see Wiley, 1981) appropriate to these philosophically Methods and rationale disparate but complementary approaches were used in the elucidation of phylogeny. A subsequent The structure and rationale for the Workshop (de- step taken by several Working Groups was a pre- scribed in detail previously by Hoberg et al., 1997a) liminary examination of host-parasite cospeciation. are again outlined briefly. The Workshop was novel in attempting to act as a catalyst for development of a synoptic phylogeny for the Eucestoda. Seven working groups, including 38 participants from 19 countries (Appendix 1), were established in Octo- ber 1995 to represent: (1) relationships at the level H o b e r g , Ga r d n e r & Ca m p b e l l , Sy s t e m a t i cs o f t h e Eu c e s t o d a 3

Results of the workshop within specific orders that are briefly reviewed here and presented in this current issue of Systematic Higher-level, inter-ordinal phylogeny Parasitology. In most instances these represent the first attempt at phylogenetic reconstruction using Advances in our understanding of the relation- cladistic methods at the intraordinal level for ces- ships among the currently recognised orders of todes. Bray, Jones & Hoberg (this issue) address the the Eucestoda were achieved based on indepen- phylogeny of the Pseudophyllidea and examine the dent approaches linked to comparative morphol- structure of the group with respect to subordinal ogy (Hoberg et al., 1997b), evaluation of sperma- systematics and taxonomy. Beveridge, Campbell tozoon ultrastructure and spermiogenesis (Justine, & Palm (this issue) examined the genera of the try- 1998) and analysis of sequence data from 18S rDNA panorhynchs, present a preliminary phylogeny and (Mariaux, 1998) (Figures 1,2). Parsimony analysis attempt to evaluate and initiate resolution among of morphological and molecular data bases yielded the currently competing hypotheses for systemat- largely congruent trees supporting monophyly for ics of the group (e.g. Campbell & Beveridge, 1994; the Eucestoda. Within the Eucestoda, the monozoic Palm, 1997). Ivanov & Hoberg (this volume) exam- Caryophyllidea van Beneden in Carus, 1863 are ined the problematical Diphyllidea and present a the basal taxon; difossate forms such as the Pseu- preliminary phylogeny at the species level for this dophyllidea are regarded as primitive; tetrafossate enigmatic group. Rego et al. (1998), presented a ro- groups including the paraphyletic “Tetraphyllidea”, bust hypothesis for the Proteocephalidea that sup- Lecanicephalidea Baylis, 1920, Proteocephalidea, ports diagnosis of the subfamilies and monophyly Nippotaeniidea Yamaguti, 1939, Tetrabothriidea of the Monticelliidae La Rue, 1911; historical bio- Baer, 1954 and Cyclophyllidea are highly derived. geographic relationships centring on Gondwana- These hypotheses differed in the placement of two land are outlined. An hypothesis for relationships taxa, the Trypanorhyncha and Diphyllidea van among the genera of tetraphyllidean, lecanicepha- Beneden in Carus, 1863. Significantly, “total -evi lidean and diphyllidean tapeworms, based on a dence” analysis, now in progress, combining the bottom-up analysis examining representative spe- molecular and morphological data bases resolves cies and genera, was developed by Caira, Jensen & the placement of the Trypanorhyncha as depicted in Healy (1999); this will be presented in a separate the morphologically based tree (Figure 1) (Hoberg issue of Systematic Parasitology. Finally, the rela- & Mariaux, unpublished data). Additionally, mo- tionships of the families within the Cyclophyllidea lecular studies suggest that the Mesocestoididae were studied by Hoberg, Jones & Bray (this issue), Perrier, 1897 is the sister-group of the Tetraboth- with the results of this analysis being compared to riidea + Cyclophyllidea (Mariaux, 1998). Conse- molecular level investigations by Mariaux (1998). quently, the application of comparative data from These series of papers form the core of the results, morphology, ontogeny and ultrastructure is vali- dealing with inter-and intra-ordinal relationships dated and the complementary nature of morpho- from the 2nd IWTS. Each presents an historical logical and molecular approaches is emphasised. treatment of a respective group, identification and As such, these higher-level analyses may form a discussion of characters, phylogenetic reconstruc- robust foundation for eventual complete resolution, comparison with prior explicit phylogenetic tion of inter-ordinal phylogeny for the tapeworms. hypotheses and in some cases discussion of co- These analyses also serve to highlight the continued speciation and historical biogeography. Also em- problematical nature of relationships among tetra- phasised are the current gaps in knowledge that fossates, particularly the coordinate Tetraphyllidea impede progress in resolution of phylogeny of and Lecanicephalidea (Hoberg et al., 1997b; also see the tapeworms and proposals for future studies. Caira et al., 1999); broader interpretations and implications of these studies are presented in Hoberg Discussion et al. (1997b), Justine (1998) and Mariaux (1998). Current state of knowledge Intra-ordinal phylogeny Higher level analyses, briefly outlined above, pro- Monophyly for the Eucestoda has been established vided the context and hierarchical basis for more in- through a number of studies based on compara- clusive studies of families, subfamilies and genera tive morphology and ultrastructure (e.g. Ehlers, 4 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12.

Figure 1. Phylogenetic hypothesis for the orders of the tapeworms derived from comparative morphology (based on Hoberg et al., 1997b). Shown is the single most parsimonious tree, an hypothesis based on 51 transformation series representing binary and multistate characters for 2 outgroups and 12 orders (the Tetraphyllidea is represented by the Phyllobothriidae and Onchobothrii- dae); Length = 151; CI = 0.815. To reconcile with the results of 18s analysis requires 16 additional steps (CI = 0.74).

1985, 1986; Brooks et al., 1985; 1991; Brooks, 1989; to resolving the numerous conflicting hypotheses Justine, 1991). Starting in 1991, studies began to fo- that have been formulated since the 19th century. cus on the relationships within the Eucestoda with Testable hypotheses, based on cladistic analyses, the first examination of the phylogenetic structure have been presented that are now open to critical for the major lineages of the tapeworms (Brooks et examination and further modification (Hoberg et al., 1991; Brooks & McLennan, 1993). Phylogenetic al., 1997b; Caira et al., 1999; Mariaux, 1998). These hypotheses for inter-ordinal relationships based on hypotheses can be used to evaluate the diversity of morphology (Hoberg et al., 1997b), ultrastructure concepts for relationships that have been presented (Justine, 1998) and molecular sequence data (Mari- in the literature and to focus on significant issues re- aux, 1998) have led to a modification of these recent lated to character evolution. Definitive resolution of concepts and earlier ideas that had been developed higher-level relationships will follow from a contin- over the past century (summarised in Hoberg et al., ued refinement of databases, inclusion of all orders 1997b). Congruence in morphological and molecu- and broader taxonomic representation in molecular approaches exemplified by the current higher- lar studies, and eventual analysis of total evidence. level analyses suggests that we are converging on a Studies based on morphology outlined herein robust understanding of evolutionary relationships have relied largely on the higher level structure among the tapeworms (Figures 1,2). Although es- revealed in top-down analysis as the basis for out- timating the phylogeny of the tapeworms has, in group selection and character polarisation (Hoberg the past, been problematical, we now may be close et al., 1997b). In this regard, however, it is critical to H o b e r g , Ga r d n e r & Ca m p b e l l , Sy s t e m a t i cs o f t h e Eu c e s t o d a 5

Figure 2. Phylogenetic hypothesis for the orders of the tapeworms derived from an analysis of sequence data representing 188 in- formative characters (from 1,102 base pairs) of 18S rDNA (based on Mariaux, 1998). Shown is a summary of higher-level relationships derived from a majority rule consensus tree that was based on 480 equal length phylogenetic trees. Included in the analysis were 2 outgroups and 10 orders (Haplobothriidea and Lecanicephalidea are not included) represented by 47 species-level taxa (length = 704 steps; CI = 0.41) (Mariaux, 1998); to reconcile with the results of the analysis based on comparative morphology requires 20 additional steps (CI = 0.40).

note the com plementary nature of top-down ver- Caira et al., 1999; Ivanov & Hoberg, 1999; Hoberg et sus bottom-up approaches that rely on sampling al., 1999; Rego et al., 1998). Prior to the Workshop, of representative taxa (e.g. Caira et al., 1999) and only the Tetrabothriidea (Hoberg, 1989; Hoberg & to recognise that in both instances the goal is to re- Adams, 1992) and the Proteocephalidea (Brooks, construct the phylogenetic history for a group. Hy- 1978; Brooks & Rasmussen, 1984) had been evalu- potheses are presented as a potential stimulus for ated. The Haplobothriidea Joyeux & Baer, 1961, more detailed discussion that embodies a diversity Nippotaeniidea, Caryophyllidea and Spathebothri- of views and contributions. Phylogenetic resolution idea Wardle & McLeod, 1952 have yet to be exam- has now been obtained for inter-ordinal relation- ined in detail with modern phylogenetic methods. ships among the eucestodes. During the 2nd IWTS, Hopefully, the stage may be set for continued hypotheses varying in their degrees of resolution and rapid advances in our understanding of the were developed for families, subfamilies or genera relationships among the eucestodes. These stud- among seven of 12 recognised orders (Pseudophyl- ies have also served to re-emphasise the rich ge- lidea, Diphyllidea, Trypanorhyncha, “Tetraphyl- nealogical diversity of the tapeworms and to raise lidea”, Lecanicephalidea, Proteocephalidea and Cy- intriguing questions about their co-evolutionary clophyllidea) (Beveridge et al., 1999; Bray et al., 1999; linkages with vertebrate and invertebrate hosts. 6 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12.

Higher-level relationships and co-evolution parasite taxa (Figure 3); data for host-distribution are primarily from Schmidt (1986). The gyrocotylid- It has long been recognised that the tapeworms are eans are restricted to Holocephala among the chon- an archaic group, and this has been emphasised by drichthians, whereas the amphilinideans are found concepts for host-parasite associations and the puta- in basal actinopterygians (Acipenseridae, sturgeons) tive role of co-evolution (collectively, co-speciation and probably secondarily in basal teleosts (e.g. os- and co-adaptation, see Brooks & McLennan, 1991) teoglossomorph fishes) and chelonians; notably the in the development of groups and assemblages (e.g. basal species of amphilinideans, Amphilina folia- Lönnberg, 1897; Fuhrmann, 1931; Wardle & McLeod, cea (Rudolphi, 1819) and A. japonica Goto & Ishi, 1952). These studies generally concluded that prim- 1936 are parasites in sturgeons (Brooks & McLen- itive chondrichthians were hosts for ancestral taxa nan, 1993). In contrast, members of the basal taxon of eucestodes. Phylogenetically based assessments in the eucestodes, Caryophyllidea, are restricted to of eucestode evolution, however, suggested that families of freshwater teleosts (e.g. the relatively ancestral groups of tapeworms were parasites in te- basal Catostomidae, Cyprinidae and Siluriformes). leost fishes (Brookset al., 1991; Hoberg et al., 1997b). Spathebothriideans are found in sturgeons and A more comprehensive examination of this hypoth- teleosts (Salmonidae and Percidae). Pseudophyl- esis (outlined below) may indicate an association lideans are found in some actinopterygians (e.g. with earlier and basal actinopterygian fishes. Dis- Marsipometra Cooper, 1917 in the paddlefish Poly- course, however, on the implications of this obser- odon spathula and Eubothrium Nybelin, 1922 in vation and the putative age and early radiation of sturgeons), but principally in marine and freshwa- tapeworms in vertebrate host taxa has been limited. ter teleosts. The limited presence of some pseudo- A co-evolutionary history and radiation of the phyllideans in amphibians (Cephalochlamydidae eucestodes may involve temporally deep co-spe- Yamaguti, 1959), chelonians (a species of Triaeno- ciation with vertebrate host taxa accompanied by phoridae Lönnberg, 1889), lepidosaurians (liz- some level of secondary colonisation (e.g. Hoberg ards and snakes), and aquatic birds and mammals et al., 1997b; Hoberg et al., 1999) (Figure 3) and may (Diphyllobothriidae Lühe, 1902) may represent sec- extend at a minimum into the Palaeozoic, to 350– ondary episodes of colonisation. Haplobothriideans 420 million years before present (mybp). Alterna- are parasites in the bowfin Amia calva, a neoptery- tively, some ordinal-level taxa could be younger gian, basal to the teleosts. The diphyllideans, try- than this minimum if recent colonisation, in con- panorhynchs and the paraphyletic assemblage of trast to temporally deep host-switching, has been a the tetraphyllideans along with the lecanicephalid- dominant force in diversification. Such hypotheses eans are found exclusively in chondrichthians (Ne- can be evaluated within the context of parasite and oselachii, skates, rays and sharks). Proteocephalide- host phylogeny, host distribution for parasites, his- ans are found principally in Siluriformes (catfishes) torical biogeography and the fossil record for ver- but also other relatively basal freshwater teleosts; tebrates (Brooks & McLennan, 1993; Hoberg, 1997). some proteocephalideans are known in amphib- The relationships for the Gyrocotylidea Poche, ians, chelonians and lepidosaurians (Rego et al., 1926, Amphilinidea Poche, 1922 and Eucestoda 1998). Nippotaeniideans are parasites in basal te- provide the context for elucidating early host-para- leosts (e.g. galaxids). The sister taxa Tetrabothriidea site associations. The gyrocotylideans are the sister- and Cyclophyllidea are the only groups that pre- group of the amphilinideans + eucestodes, and the dominate in avian and mammalian hosts, although former taxa are recognised as relictual groups that a restricted number of genera and species in the lat- diversified prior to the breakup of Pangea (Bandoni ter are found in amphibians, chelonians and lepido- & Brooks, 1987a,b; Brooks & Bandoni, 1988). A sis- saurians (Figure 3). Notably, the tetrabothriideans ter-group relationship for the amphilinideans and are limited in occurrence in seabirds, pinnipeds and tapeworms suggests a minimum age in excess of 200 cetaceans. Additionally, the mesocestoidids, a pu- mybp and indeed, as outlined below, these groups tative relictual group restricted to carnivores, may appear to be considerably older, based on assump- be the sister group for the Tetrabothriidea + Cyclo- tions of host-parasite co-speciation at a basal level. phyllidea (see Hoberg et al., 1999; Mariaux, 1998). Clear patterns of host-associations are evident If basal co-speciation is a viable assumption, we relative to the distribution of extant vertebrate and can use this information to infer a minimum age for H o b e r g , Ga r d n e r & Ca m p b e l l , Sy s t e m a t i cs o f t h e Eu c e s t o d a 7

Figure 3. Phylogenetic hypothesis for eucestodes based on comparative morphology, showing the distribution of major vertebrate definitive hosts. Host-taxa were mapped and optimised on the tree representing the complete analysis including all ordinal level taxa, with MacClade 3.05 (Maddison & Maddison, 1995); CI = 0.94, RI = 0.83. Host distributions are indicative of an early co-evolutionary association with basal actinopterygian fishes, multiple colonisations of relatively basal teleosts, and a secondary colonisation of chondrichthians, compatible with a complex history of co-speciation, host-switching and extinction. Host taxa are as follows: A = avian groups; Ac = basal actinopterygians (e.g. sturgeons, the bowfinAmia calva and paddlefishPolyodon spathula); Am = amphibians; Ce = chelonians; Ch1 = holocephalans or chimaeras (Chondrichthyes); Ch2 = neoselachians, or sharks, skates and rays (Chondrichthyes); L = lepidosaurians (snakes and lizards); M = mammals; and T = basal teleosts. the true tapeworms. It must be recognised, however, as the Devonian 420 mybp. Gyrocotylideans then that origin or basal cladogenesis for a group may be represent the remnants of a radiation in chondrich- radistinct from secondary radiation within a clade thians that ultimately survived in the Holocephala. that accounts for currently extant genera and spe- In contrast, the amphilinideans + eucestodes cies, and perhaps families. The basal groups of euc- apparently diversified initially in primitive ray- estodes, as noted above, are primarily found in basal finned fishes. This is compatible with the- earli actinoptery gian and relatively basal teleost fishes; est radiation of tapeworms being associated with there is no indication based on the parasite phylog- actinopterygian and neopterygian fishes after eny and mapping of host groups that eucestodes 350–400 mybp, in lineages including sturgeons, were present in archaic sharks and rays, although paddlefish and bowfins, with secondary host gyrocotylideans are present in holocephalans. Cla- switches to basal teleosts, chondrichthians (neo- dogenesis leading to the gyrocotylideans and am- selachians), amphibians and amniotes (see Brooks philinideans + eucestodes may have coincided with et al., 1991; Hoberg et al., 1997b) (Figure 3). Colo- the divergence of placoderms + chondrichthians nisation of tetrapods is postulated based on the and lineages leading to the actinopterygians as early absence of tapeworms in lobe-fins, such as -lung 8 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12. fishes and coelacanths, although this could repre- timately went to extinction. Considering extant sent a secondary loss or extinction in these groups. eucestode taxa, the phylogenetic position of the The chondrichthians + placoderms are the sister diphyllideans and their occurrence largely in skates group for an assemblage of extinct piscine taxa + ac- and rays (Campbell & Andrade, 1997; Ivanov & tinopterygians; the ray-finned fishes contain the de- Hoberg, 1999) is compatible with an hypothesis rived teleosts (Long, 1995; Stiassny et al., 1996). The for secondary colonisation and radiation. Such fossil record indicates that initial diversification of colonisation may have coincided with the radiation the phylogenetically disparate archaic sharks and of chondrichthians (Neoselachii + Batoidea) that ray-finned fishes occurred in the Devonian about extended from the Devonian into the Mesozoic. 410– 420 mybp, with a later radiation of the holo- Interestingly, this pattern of association of euc- cephalans and sturgeons between 250–355 mybp. estodes in actinopterygians, teleosteans and chon- By the termination of the Permian, 250 mybp, the drichthians appears to be paralleled to some extent chimaeras, neoselachians and actinopterygians, by the Digenea and Monogenea. Brooks (1989) represented by the paleoniscoids with lineages suggested that initial diversification of digeneans, leading to the sturgeons, gars, paddlefish and bow- monogeneans and cestodarians coincided with the fins, are recognised. Teleosts are not represented origins and divergence of lineages for chondrich- until the Triassic (after 250 mybp) and all major or- thians and Osteichthyes. Boeger & Kritsky (1997) ders are present by the mid-Cretaceous, covering a have postulated that there was a radiation of mono- span of 100–250 mybp. The basal amphibians are geneans in early chondrichthians that largely went recognized in the late Devonian, and three lineages extinct and that extant groups of parasites in neo- of amniotes, represented by mammals (synapsids), selachians represent a colonisation from teleosts. In chelonians and saurian groups (leading to birds), the case of the Digenea, their sister group, the aspi- diverged in the upper Carboniferous, 300 mybp; dogastreans, is also relictual, with basal members mammals originated in the Triassic at 225 mybp in chondrichthians and occasionally other aquatic and birds in the mid-Jurassic, 160 mybp (see Car- hosts. In contrast to cestodes and monogeneans, roll, 1988; Dingus & Rowe, 1998). This provides a very few digeneans have colonised sharks and rays. minimum putative age for the diversification of The putative great age for eucestodes in basal eucestodes in vertebrates, assuming a basal asso- actinopterygian, teleostean and chondrichthian ciation of ancestral tapeworms with actinoptery- fishes is further compatible with estimates for the gian fishes, and the basis for examining patterns timing of diversification of tapeworms, including of development for host-parasite associations. the tetrabothriideans and cyclophyllideans, which Ray-finned fishes as the basal hosts for tape- are dominant respectively in marine and terrestrial worms suggests that the occurrence of caryophyl- birds and mammals (Spasskii, 1993a,b; Hoberg et lideans, spathebothriideans, pseudophyllideans al., 1999). The postulated ancestor of the tetraboth- and proteocephalideans + nippotaenideans in te- riideans + cyclophyllideans may have been a para- leosts is attributable to colonisation (Figure 3). This site in late Palaeozoic or early Mesozoic synapsids contention is further supported by the distribu- or saurians. The distribution in contemporary host tion of these cestodes in relatively basal groups of groups suggests diversification of tetrabothriideans teleosts (Long, 1995; Lauder & Wainwright, 1992). in now extinct marine saurians (e.g. ichthyosaurs) Thus, it is postulated that there were four inde- and non-avian archosaurs (e.g. pterosaurs), early pendent episodes of colonisation by eucestodes in colonisation of seabirds in the late Cretaceous and freshwater and marine teleostean fishes (Figure 3). secondary host-switching to marine mammals in the It further suggests that the radiation of tapeworm Tertiary (Hoberg & Adams, 1992; Spasskii, 1993b; lineages limited in distribution to contemporary Hoberg et al., 1997b). This would further suggest sharks and rays resulted from colonisation via an that the initial diversification of cyclophyllideans actinopterygian source early in the diversification occurred in now extinct terrestrial saurians or syn- of neoselachians to account for the considerable apsids during the early Mesozoic, with colonisation genealogical and ecological diversity observed in or co-evolution in early mammals and colonisation such taxa as the trypanorhynchs and “tetraphyl- of amphibians after 225 mybp (see Dingus & Rowe, lideans” (Figure 3). In this context, the gyrocotyl- 1998). In this context, the basal cyclophyllideans ideans in chimaeras appear as relictual remnants are represented by the Mesocestoididae + Nemato- of an early radiation in chondrichthians that ul- taeniidae Lühe, 1910, the latter group having radi- H o b e r g , Ga r d n e r & Ca m p b e l l , Sy s t e m a t i cs o f t h e Eu c e s t o d a 9 ated in gondwanan anurans 180–200 mybp (Jones, mental perturbation (e.g. Gardner & Campbell, 1987; Hoberg et al., 1999). Consequently, the current 1992; Hoberg, 1997; Hoberg et al., 1999). It may be distribution of these tapeworm taxa may be, in part, remarkable that tapeworms with complex life-cy- related to patterns of colonisation of mammals and cles, dependent on phylogenetically disparate ver- birds and extinction of ancestral host lineages during tebrate and invertebrate hosts, were persistent. It is the Mesozoic (Spasskii, 1993a,b; Hoberg et al., 1999). apparent, however, that parasite-host assemblages The depauperate tapeworm faunas or the spo- have tracked across extinction events that may have radic occurrence of phylogenetically unrelated been of global proportions. Extinction-bottlenecks cestodes in amphibians, chelonians and lepidos- would have been determinants of parasite diversity aurians (snakes and lizards) and their absence in relative to elimination of host groups or particular lobe-finned fishes (coelacanths and lung fishes) parasite taxa; repeated bottlenecks and secondary and crocodilians is consistent with an hypothesis radiation for survivors may explain the current pat- for independent colonisation following divergence terns of host associations, and genealogical and eco- of respective tetrapod host groups in the Palaeo- logical diversity for eucestodes. Additionally, the zoic and Mesozoic. This observation is particu- distribution of some taxa suggests diversification larly highlighted by the distribution of tapeworms in synapsids, saurians and non-avian archosaurs in turtles (Pichelin et al., 1998) and amphibians. that became extinct subsequent to colonisation of Overall, the patterns of occurrence for cestodes now recognised contemporary host groups such as are suggestive of a series of colonisation episodes birds and mammals. The implications are appar- accompanied by rapid and explosive radiations ent for understanding the continuity of ecological in fishes (e.g. neoselachians and relatively basal structure over evolutionary time frames, within the teleosts) and amniotes (e.g. in lineages leading context that the persistence of parasite lineages is to extant birds and mammals) over short time intimately dependent upon host-group survival, frames coinciding with the origins of respective and stability of host-parasite assemblages. Thus, host groups. Following an early co-evolutionary cestodes serve to provide the linkage for examin- history with basal actinopterygians, the temporal ing the interaction of co-evolution, colonisation duration of these associations potentially extends and extinction on the structure of faunas and eco- from the middle to late Palaeozoic and or early logical continuity across deep temporal and geo- Mesozoic into the Tertiary, with the development graphical scales (Hoberg, 1997; Hoberg et al., 1999). of specific assemblages being dependent on the timing of host-switching (see Hoberg et al., 1999). Conclusions and the future An implication of a deep and complex history for eucestodes is the observation that these groups were Phylogenetic studies of tapeworms derived from persistent across major global extinction events that the 2nd IWTS place the eucestodes among the best- marked the termination of the Permian 250 mybp resolved taxa. Congruence is apparent in compre- and the Cretaceous 65 mybp (Alvarez et al., 1980; hensive inter-ordinal hypotheses that have thus far Bowring et al., 1998), inclusive in the seven to nine been developed (e.g. Hoberg et al., 1997b; Mariaux, episodes that have been defined for the Phanerozoic 1998). Phylogenetic assessments for relationships (see Briggs, 1995). Lineage persistence may have within eight orders have been presented since 1989, involved all of the currently recognised orders for with seven new studies being generated from the the eucestodes. The alternative, which appears less 2nd IWTS. The stage is set for rapid advances in likely, is that major lineages of cestodes originated our understanding of the evolutionary history of and radiated subsequent to these extinction events; the Eucestoda. Progress is dependent on identi- there is no indication, however, of orders originating fication of gaps in our knowledge (e.g. Mariaux, subsequent to the Cretaceous-Tertiary boundary. 1996), recognition of new characters and new con- Assuming the estimate of a middle to late Palaeo- cepts for interpretation, as exemplified by the di- zoic age for tapeworms is correct, it is apparent from verse studies presented in this issue of Systematic an historical ecological perspective (Brooks, 1985) Parasitology. The ultimate goal is for resolution of that faunal assemblages represented by definitive phylogeny based on assessment of total evidence, and intermediate hosts and particular tapeworm derived from a diversity of data-sets, including taxa can serve as indicators of ecological structure morphological characters and multiple gene sys- and stability during periods of maximal environ- tems to achieve new insights based on the applica- 10 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12. tion of a unified methodology for analysis. We ap- pha). Canadian Journal of Zoology, 65, 1,110–1,128. pear to be in reach of this goal (Hoberg et al., 1997a). Bandoni, S.M. & Brooks, D.R. (1987b) Revision and phylogenetic analysis of the Gyrocotylidea Poche, 1926 This is a tumultuous time as we approach the end (Platyhelminthes: Cercomeria: Cercomeromor- of the 20th Century. We have the opportunity, how- pha). Canadian Journal of Zoology, 65, 2,369–2,389. ever, to provide a new, solid foundation and direc- Beveridge, I., Campbell, R.A. & Palm, H.W. (1999) Prelimi- tion for advances in cestode systematics. The 2nd nary cladistic analysis of genera of the cestode order Try- IWTS has contributed a strong level of continuity panorhyncha Diesing, 1863. Systematic Parasitology, 42, 22–49. Boeger, W.A. & Kritsky, D.C. (1997) Coevolution of for scientific progress, basic research and education. the Monogenoidea (Platyhelminthes) based on a re- The commitments to the success of the 2nd IWTS on vised hypothesis of parasite phylogeny. Inter- the part of all participants has served to promote national Journal for Parasitology, 27, 1,495–1,511. continuing advances in understanding tapeworm Bowring, S.A., Erwin, D.H., Jin, Y.G., Martin, M.W., Davidek, K. & Wang, W. (1998) U/Pb zircon geochronology and tempo biodiversity, evolution and elucidation of a com- of the end-Permian mass extinction. Science, 280, 1,039–1,048. plex history for biogeography and co-evolution. Bray, R.A., Jones, A. & Hoberg, E.P. (1999) Observations on the phylogeny of the cestode order Pseudophyl- Acknowledgements lidea Carus, 1863. Systematic Parasitology, 42, 13–20. Briggs, J.C. (1995) Global Biogeography. New York: Elsevier, 452 pp. The 2nd IWTS, organised by EPH, SLG and RAC, Brooks, D.R. (1978) Evolutionary history of the cestode or- was held at the Harold W. Manter Laboratory der Proteocephalidea. Systematic Zoology, 27, 312–323. Brooks, D.R. (1985) Historical ecology: a new approach of Parasitology, University of Nebraska-Lincoln to studying the evolution of ecological associations. 2–6 October 1996, with the theme of promoting a Annals of the Missouri Botanical Garden, 72, 660–680. broad-based phylogenetic research programme on Brooks, D.R. (1989) A summary of the database pertaining to the cestodes. Thirty-eight scientists representing 19 phylogeny of the major groups of parasitic platyhelminthes, with countries participated, including nearly all current a revised classification.Canadian Journal of Zoology, 67, 714– 720. Brooks, D.R. & Bandoni, S.M. (1988) Coevolu- world authorities on cestode taxonomy and char- tion and relicts. Systematic Zoology, 37, 19–33. acter analysis. We sincerely thank the participants Brooks, D.R., Hoberg, E.P. & Weekes, P.J. (1991) Preliminary who freely shared their knowledge and ideas, over phylogenetic systematic analysis of the major lineages of many long hours, resulting in a truly synergis- the Eucestoda (Platyhelminthes: Cercomeria). Proceed- ings of the Biological Society of Washington, 104, 651–668. tic workshop. We acknowledge the efforts of Niki Brooks, D.R. & McLennan, D.A. (1991) Phylogeny, Ecol- Gulseth and Mauritz ‘Skip’ Sterner, of the Harold ogy and Behavior: A Research Program in Comparative Bi- Manter Laboratory, and Judith Holland of the Bio- ology. Chicago: University of Chicago Press, 434 pp. systematics and National Parasite Collection Unit, in Brooks, D.R. & McLennan, D.A. (1993) Parascript Par- ensuring a productive meeting. The Workshop was asites and the Language of Evolution. Washing- ton, DC: Smithsonian Institution Press, 429 pp. generously supported by grants and other resources Brooks, D.R., O’Grady, R.T. & Glenn, D.R. (1985) The phylog- from the American Society of Parasitologists, Ag- eny of the Cercomeria Brooks, 1982 (Platyhelminthes). Pro- ricultural Research Service (Office of the Director, ceedings of the Helminthological Society of Washington, 52, 1–20. Beltsville Area Research Center; and BNPCU), Uni- Brooks, D.R. & Rasmussen, G. (1984) Proteocephalid cestodes from Venezuelan catfish, with a new classification of the Monticellii- versity of Nebraska-Lincoln (H.W. Manter Labora- dae. Proceedings of the Biological Society of Washington, 97, 748–760. tory; and Office of the Chancellor), Foreign Agri- Caira, J.N., Jensen, K. & Healy, C.J. (1999) On the phy- cultural Service, USDA, the United States Civilian logenetic relationships among the tetraphyllid- Research and Development Foundation (CRDF) for ean, lecanicephalidean, and diphyllidean tape- the Independent States of the Former Soviet Union, worm genera. Systematic Parasitology, 42, 77-151. Campbell, R.A. & Andrade, M. (1997) Echinobothrium raschii n. sp. Pfizer Inc., and private donations. We also thank (Cestoda: Diphyllidea) from Rhinoraja longi (Chondrichthyes: Deborah McLennan and Daniel Brooks for critical Rajoidei) in the Bering Sea. Journal of Parasitology, 83, 115–120. comments on ideas presented in this manuscript. Campbell, R.A. & Beveridge, I. (1994) Order Trypano- rhyncha Diesing, 1863. In: Khalil, L.F., Jones, A. & Bray, R.A. (Eds) Keys to the Cestode Parasites of Verte- References brates. Wallingford, UK: CAB International, pp. 51–148. Alvarez, L.W., Alvarez, W., Asaro, F. & Michel, Carroll, R.L. (1988) Vertebrate Paleontology and Evo- H.V. (1980) Extraterrestrial cause for the Creta- lution. New York: W. H. Freeman, 698 pp. ceous-Tertiary extinction. Science, 208, 1,095–1,108. Dingus, L. & Rowe, T. (1998) The Mistaken Extinction, Dinosaur Evo- Bandoni, S.M. & Brooks, D.R. (1987a) Revision and phy- lution and the Origin of Birds. New York: W.H. Freeman, 332 pp. logenetic analysis of the Amphilinidea Poche, 1922 Ehlers, U. (1985) Phylogenetic relationships among the Platy- (Platyhelminthes: Cercomeria: Cercomeromor- helminthes. In: Morris, C., George, J.D., Gibson, R. & Platt, H o b e r g , Ga r d n e r & Ca m p b e l l , Sy s t e m a t i cs o f t h e Eu c e s t o d a 11

H.M. (Eds), The Origins and Relationships of Lower Inverte- Maddison, W.P. & Maddison, D.R. (1995) MacClade: Analy- brates. Oxford, UK: Oxford University Press, pp. 143–158. sis of Phylogeny and Character Evolution. Version 3.05. Ehlers, U. (1986) Comments on a phylogenetic sys- Sunderland, Massachusetts: Sinauer & Associates. tem of the Platyhelminthes. Hydrobiologia, 132, 1–12. Mariaux, J. (1996) Cestode systematics: any prog- Fuhrmann, O. (1931) Dritte Klasse des Cladus Platyhelmint- ress? International Journal for Parasitology, 26, 231–243. hes. Cestoidea. In: Kukenthal, W. (Ed.) Handbuch der Zo- Mariaux, J. (1998) A molecular phylogeny of the Eu- ologie.Vol. 2. Berlin: Kukenthal und Krumbach, pp. 141–416. cestoda. Journal of Parasitology, 84, 114–124. Hennig, W. (1966) Phylogenetic Systematics. Ur- Mariaux, J. & Vaucher, C. (1994) Progress in tape- bana, Illinois: University of Illinois Press, 263 pp. worm systematics. Parasitology Today, 10, 43–44. Gardner, S.L. & Campbell, M.L. (1992) Parasites as probes Palm, H. (1997) An alternative classification of trypano- for biodiversity. Journal of Parasitology, 78, 596–600. rhynch cestodes considering the tentacular armature as be- Hoberg, E.P. (1989) Phylogenetic relationships ing of limited importance. Systematic Parasitology, 37, 81–92. among the genera of the Tetrabothriidae (Eu- Pichelin, S., Cribb, T.H. & Bona, F.V. (1998) Glossocercus chelodi- cestoda). Journal of Parasitology, 75, 617–626. nae (MacCallum, 1921) n. comb. (Cestoda: Dilepididae) from Hoberg, E.P. (1997) Phylogeny and historical reconstruc- freshwater turtles in Australia and a redefinition of the genus tion: Host parasite systems as keystones in biogeogra- Bancroftiella Johnston, 1911. Systematic Parasitology, 39, 165–181. phy and ecology. In: Reaka-Kudla, M.L., Wilson, D. & Rego, A.A., de Chambrier, A., Hanzelova, V., Hoberg, E., Wilson, E.O. (Eds) Biodiversity II: Understanding and Pro- Scholz, T., Weekes, P. & Zehnder, M. (1998) Prelimi- tecting Our Biological Resources. Washington, DC: Joseph nary phylogenetic analysis of subfamilies of the Proteo- Henry Press, National Academy of Sciences, pp. 243–261. cephalidea (Eucestoda). Systematic Parasitology, 40, 1–19. Hoberg, E.P. & Adams, A. (1992) Phylogeny and historical biogeog- Schmidt, G.D. (1986) CRC Handbook of Tapeworm raphy and ecology of Anophryocephalus spp (Eucestoda: Tet- Identification. Boca Raton: CRC Press, 675 pp. rabothriidae) among pinnipeds of the Holarctic during the late Spasskii, A.A. (1993a) [On the cestode fauna of the Me- Tertiary and Pleistocene. Canadian Journal of Zoology, 70, 703–719. sozoic terrestrial dinosaurs.] Conference XI, Ukrainian Hoberg, E.P., Gardner, S.L. & Campbell, R.A. (1997a) Paradigm Society of Parasitologists, Kiev. Tezisy Dokladov, pp. shifts and tapeworm systematics. Parasitology Today, 13, 161– 162. 152–153. (In Russian; English translation by V. Tkach). Hoberg, E.P., Jones, A. & Bray, R.A. (1999) Phylogenetic analysis Spasskii, A.A. (1993b) [On the participation of the marine Me- among the families of the Cyclophyllidea (Eucestoda) based sozoic reptiles in the evolution of the suborder Tetrabo- on comparative morphology, with new hypotheses for co- thriata (Cestoda: Tetraphyllidea).] Conference XI, Ukrai- evolution in vertebrates. Systematic Parasitology, 42, 51–73. nian Society of Parasitologists, Kiev. Tezisy Dokladov, Hoberg, E.P., Mariaux, J., Justine, J.-L., Brooks, D.R. & pp. 153–154. (In Russian; English translation by V. Tkach). Weekes, P.J. (1997b) Phylogeny of the orders of the Eu- Stiassny, M.L.J., Parenti, L. & Johnson, G.D. (Eds) (1996) The In- cestoda (Cercomeromorphae) based on comparative terrelationships of Fishes. New York: Academic Press, 496 pp. morphology: historical perspectives and a new work- Swofford, D.L. (1993) PAUP: Phylogenetic Analysis Using Parsimony. ing hypothesis. Journal of Parasitology, 83, 1,128–1,147. Version 3.1.1. Champaign, Ill.: Illinois Natural History Survey. Ivanov, V. & Hoberg, E.P. (1999) Preliminary comments Wardle, R.A. & McLeod, A.J. (1952) The Zoology of Tape- on a phylogenetic study of the order Diphyllidea van worms. Minneapolis: University of Minnesota Press, 780 pp. Beneden in Carus, 1863. Systematic Parasitology, 42, 21–27. Wiley, E.O. (1981) Phylogenetics: The Principles and Practice of Phy- Jones, M.K. (1987) A taxonomic revision of the logenetic Systematics. New York: John Wiley & Sons, 439 pp. Nematotaeniidae Lühe, 1910 (Cestoda: Cyclo- Wiley, E.O., Siegel-Causey, D., Brooks, D.R. & Funk, V. (1991) The phyllidea). Systematic Parasitology, 10, 165–245. Compleat Cladist: a Primer of Phylogenetic Procedures. Lawrence, Justine, J.-L. (1991) Phylogeny of parasitic Platyhelmint- Kansas: University of Kansas Museum of Natural History, 158 pp. hes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and sperm. Canadian Journal of Zoology, 69, 1,421–1,440. Justine, J.-L. (1998) Spermatozoa as phylogenetic characters for the Eucestoda. Journal of Parasitology, 84, 385–408. Appendix 1 Khalil, L.F., Jones, A. & Bray, R.A. (Eds) (1994) Keys to the Cestode Par- asites of Vertebrates. Wallingford, UK: CAB International, 751 pp. Participants in the Second International Workshop Lauder, G.V. & Wainwright, P.C. (1992) Function and history: the pharyngeal jaw apparatus in primitive ray- for Tapeworm Systematics, listing national affilia- finned fishes. In: Mayden, R.L. (Ed.) Systematics, His- tion and area of expertise. torical Ecology, and North American Freshwater Fishes. Stanford, CA: Stanford University Press, pp. 455–471. Australia: Ian Beveridge (Cyclophyllidea – Anoplo- Lönnberg, E. (1897) Beitrage zur Phylogenie der cephalidae; Tetraphyllidea; Trypanorhyncha). Ar- Platyhelminthen. Centralblatt Bakteriologie Para- sitenkunde und Infektionkrankheiten, 21, 674–684. gentina: Veronica Ivanov (Tetraphyllidea; Diphyl- Long, J.A. (1995) The Rise of Fishes: 500 Million Years of Evolu- lidea. Brazil: Amilcar Rego (Proteocephalidea tion. Baltimore: Johns Hopkins University Press, 223 pp. – working group chair). Bulgaria: Boyko Georgiev Maddison, W.P., Donoghue, M.J. & Maddison, D.R. (1984) Out- (Cyclophyllidea, Metadilepididae, Paruterinidae group analysis and parsimony. Systematic Zoology, 33, 83–103. 12 S y s t e m a t i c Pa r a s i t o l o g y (1999), 42: 1-12.

– working group chair). Canada: Daniel Brooks1 cephalidea). Marc Zehnder2 (molecular systemat- (higher-level systematics). Czech Republic: Tomas ics; Proteocephalidea). Ukraine: Vadim Korniushin Scholz (Proteocephalidea). France: Louis Euzet (Tet- (Cyclophyllidea, Metadilepididae, Paruterinidae, raphyllidea; higher-level cestode systematics). Jean- Hymenolepididae). Vasilij Tkach (Cyclophyllidea, Lou Justine (ultrastructural characters, spermatozo- Hymenolepididae). United Kingdom: Rodney Bray ons – working group chair). Germany: Harry Palm (Pseudophyllidea – working group chair; Cyclo- (Trypanorhyncha). Italy: Franco Bona (Cyclophyl- phyllidea). Arlene Jones (Cyclophyllidea – working lidea, Dilepididae). Korea: Keeseon S. Eom (Taeni- group chair; Pseudophyllidea). United States: Eric idae). Lithuania: Svetlana Bondarenko (Cyclophyl- P. Hoberg (higher level systematics – working group lidea, Hymenolepididae). New Zealand: Peter chair; Tetrabothriidea; Cyclophyllidea, Taeniidae). Weekes (higher-level systematics; Nippotaeniidea; Scott Gardner (Cyclophyllidea, Hymenolepidi- Proteocephalidea). Poland: Peter Swiderski1 (ultra- dae – working group chair). Robert Rausch (Cyclo- structural characters). Russia: Vladimir D. Gulyaev1 phyllidea, Taeniidae). Robin Overstreet (Tetraphyl- (higher level systematics; Cyclophyllidea). Slovak lidea). Janine Caira (Tetraphyllidea). Tim Ruhnke Republic: Vladimira Hanzelova (Proteocepha- (Tetraphyllidea). Ronald Campbell (Tetraphyllidea; lidea). Ivica Kraloval2 (Proteocephalidea; molecular Lecanicephalidea; associated orders – working systematics). Switzerland: Jean Mariaux (molecu- group chair; Trypanorhyncha). Peter Olson2 (mo- lar systematics – working group chair; higher-level lecular systematics). Tom Mattis (Tetraphyllidea). systematics; Cyclophyllidea, Dilepididae). Claude Claire Healy2 (Tetraphyllidea). Kirsten Jensen2 (Tet- Vaucher (Cyclophyllidea, Hymenolepididae –work- raphyllidea). Gaines Tyler2 (Tetraphyllidea). Mariel ing group chair). Alain de Chambrier (Proteo- Campbell (Cyclophyllidea, Anoplocephalidae).

1 Corresponded with Working Group, but could not attend 2 Graduate student observer/participant. Workshop.