Phylogeny and classification of the Digenea (Platyhelminthes ...

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752P.D. Olson et al. / International Journal for Parasitology 33 (2003) 733–755immediate explanation and should be verified by furtheranalysis.The second large clade of the Microphalloidea includestwo sub-clades: the Zoogonidae þ Faustulidae and anothercomprising the same four families that represented theMicrophalloidea in the studies of Tkach et al. (2001b, 2003).This is, as far as we are aware, the first time this relationshiphas been proposed. Most genera now housed in theFaustulidae have hitherto been considered fellodistomes,usually as belonging to the subfamily Baccigerinae (Bray,1988). Hall et al. (1999) found a close relationship offaustulids to the Zoogonidae in their molecular phylogeny.The original description of Faustula by MacCallum (1919)was erroneous in describing paired lateral vaginae (similarto the situation in some Monogenea) and led to the erectionof the ‘supersuperfamilie’ Faustulida by Poche (1926). Theredescription of Faustula by Price (1938) showed that therewas no supporting evidence for the erection of a new majortaxon. The rest of the families in this clade havetraditionally been considered closely related, althoughtheir systematic position and taxonomic status varied. Forinstance, they were grouped within the superfamiliesProsthogonimoidea and Microphalloidea in the system ofOdening (1964) and Lecithodendrioidea and Microphalloideain the system of Brooks et al. (1985, 1989).The distinct separation of the Lecithodendriidae andPleurogenidae by present molecular data supports thesystematic arrangement proposed by Odening (1959) whoremoved the subfamily Pleurogeninae from the Lecithodendriidaeand raised it to the family level. Odening’sviewpoint has been variously accepted (e.g. Sharpilo andIskova, 1989) or rejected (Yamaguti, 1971; Prudhoe andBray, 1982), but has been supported by molecular data (e.g.Tkach et al., 2001b, 2003 and herein).In some analyses (Figs. 1– 3), members of twosubfamilies of the Microphallidae, Microphallinae andMaritrematinae, were split among different clades. Insome cases Maritrema was closer to the Lecithodendriidaethan to Microphallus which fits the hypothesis of Bayssade-Dufouret al. (1993) based on the comparative analysis ofcercarial chaetotaxy. However, the recent molecularphylogenetic investigation of the Microphalloidea byTkach et al. (2003) supports the branch topology presentedon Figs. 5 and 6 in which the Microphallidae ismonophyletic.Opinions on the taxonomic status of Prosthogonimidaehave varied considerably and Mehra (1937) regarded it asubfamily of the Plagiorchiidae ( ¼ Lepodermatidae).However, the majority of authors have considered it aseparate family, and Odening (1964) went as far as to erectthe superfamily Prosthogonimoidea. Results of the presentanalysis support the viewpoint of Brooks et al. (1989) whoplaced them in the superfamily Microphalloidea, although itis unclear how they reached this conclusion based on theirmorphological phylogenetic analysis (see Cribb et al.,2001).Cercarial penetration gland openings dorsally to the oralsucker (character 31 of Cribb et al. (2001) is a featureuniformly exhibited, as far as we know, among members ofthe Apocreadiata, Lepocreadiata, Monorchiata, Opisthorchioideaand Xiphidiata, which form a nested clade within thehigher Plagiorchiida (Fig. 6). As this condition is also foundin many echinostomatoids, it may well be a synapomorphyof the larger nested clade including also the Echinostomata.4.4. Need for taxonomic revisionThe present study shows that revision of the classificationof the Digenea is warranted in order to better reflect thephylogenetic affinities of the taxa that are consistentlysupported by this and previous molecular phylogeneticstudies, as well as recent morphological estimates (e.g.Cribb et al., 2001). The traditional order Echinostomida isclearly a polyphyletic assemblage formed for taxonomicconvenience, whilst the traditional orders Plagiorchida andStrigeida are paraphyletic. Such a trichotomous schemecannot be maintained if we want digenean classification toreflect their phylogeny, and our results necessitate therecognition of a greater number of independent lineages.Several families have been found to be paraphyletic andconsideration must be made at some point as to theadvisability of making those families that are nested,synonyms of the paraphyletic ones, or of redefining theparaphyletic families. The pairs of taxa in question are theBrachylaimidae þ Leucochloridiidae, Diplostomidae þStrigeidae, Hemiuridae þ Lecithasteridae, Microscaphidiidaeþ Mesometridae, Echinostomidae þ Fasciolidae,Heterophyidae þ Opisthorchiidae, Haploporidae þAtractotrematidae, Opecoelidae þ Opistholebetidae andZoogonidae þ Faustulidae. In some cases, these actionswould amount to the reinstatement of earlier classificationsand in other cases the synonymies have been mooted before.Sinking of certain taxa (e.g. Atractotrematidae) might bewarranted immediately, whereas other taxa warrantadditional evidence prior to any taxonomic revision.More significant are the families found to be polyphyletic,Acanthocolpidae and Derogenidae. Again, greatertaxon sampling is needed to initiate major changes.However, the most obvious taxon for immediate scrutinyis probably the Acanthocolpidae, where it now appears clearthat Cableia is a basal monorchiid and not an acanthocolpid,lepocreadiid, opecoelid or enenterid as variously suggested(Bray et al., 1996). Attempts should thus be made to assessits morphology as a putative monorchiid.4.5. Missing taxa and unresolved questionsAlthough the present analyses represent the broadestsampling of Digenea to date, a group comprising over 140families (Gibson et al., 2002), a number of importantomissions remain, including the Allocreadiidae, Gymnophallidae,Liolopidae, Mesotretidae, Paramphistomidae,
P.D. Olson et al. / International Journal for Parasitology 33 (2003) 733–755 753Ptychogonimidae, Rhytidodidae and Urotrematidae. Someof these omissions are likely to be crucial to the fullelucidation of digenean phylogeny. The position of thePtychogonimidae, for example, could have major implicationsfor the estimation of the sequence of firstintermediate host acquisition in the group. The Urotrematidae,known now from fishes, could also be pivotal in ourunderstanding of the sequence of acquisition of definitivevertebrate hosts in the group. The systematics of theDigenea is still riddled with puzzles and inconsistencies atall levels that morphology has failed to resolve, but whichmay yield to molecular techniques in due course.The extraordinary diversity of the Digenea has requiredus to restrict our analyses and discussion largely to topicsconcerning their phylogeny and classification. We appreciatethat other aspects of their biology can be betterunderstood in a historical context as well, and a separatepaper gives consideration solely to the evolution ofdigenean life-cycles and their host associations in light ofthe results herein (see Cribb et al., 2003).Author’s note:Cotylogaster dinosoides should read cotylogaster basirion Fig. 3. Metadena sp. should read Siphodera vinaledwardsiion Figs. 3 and 5.AcknowledgementsOur sincere thanks to the following people who eitherprovided or assisted in the collection and identification ofspecimens: Takeshi Agatsuma (Kochi Medical School,Japan), David Blair (James Cook University, Australia),Charles Criscione (Oregon State University, USA), StephenCurran (Gulf Coast Research Laboratories, Mississippi,USA), Oksana Greben (Institute of Zoology, Kiev,Ukraine), Francis Gulland (The Marine Mammal Center,Sausalito, California, USA), Kathryn Hall (University ofQueensland, Australia), Phil Harris (University of Nottingham,England), Chris Harrod (University of Ulster, NorthernIreland), Sam Irwin (University of Ulster, NorthernIreland), David Johnston (The Natural History Museum,UK), Egil Karlsbakk (University of Bergen, Norway),Maree Koch (University of New England, Australia),Aneta Kostadinova (Bulgarian Academy of Sciences,Bulgaria), Soo-ung Lee (Halym University, South Korea),Matt Nolan (University of Queensland, Australia), RobinOverstreet (Gulf Coast Research Laboratories, Mississippi,USA), Tom Pennycott (SAC Veterinary Science Division,Scotland), Tom Platt (Saint Mary’s College, Indiana, USA),Gerard Pérez-Ponce de León (Universidad Nacional Autónomade México, México), Sylvie Pichelin (University ofQueensland, Australia), Klaus Rohde (University of NewEngland, Australia), Jilji Sitko (Moravian OrnithologicalInstitute, Czech Republic), Scott Snyder (University ofNebraska at Omaha, USA), Russell Stothard (The NaturalHistory Museum, UK) and John Walker (Sydney, Australia).Special thanks are due to Robin Overstreet and StephenCurran for hosting and providing assistance to P.D.O.during his collections at the Gulf Coast Research Laboratories.Thanks also to Arlene Jones (The Natural HistoryMuseum, UK) for her comments and corrections. Collectingwas made possible for T.H.C. and R.A.B. through thesupport of the Australian Research Council and theAustralian Biological Resources Study. V.V.T. was supportedby a grant from the European Union SysResourceProgramme during his visit to The Natural History Museumin London and by a grant from the Polish Committee forScientific Research (6 PO4C 00917). Funding and supportfor P.D.O., D.T.J.L. and this research was provided by aWellcome Trust Senior Fellowship to D.T.J.L.(043965/Z/95/Z).ReferencesBarker, S.C., Blair, D., Cribb, T.H., Tonion, K., 1993. Phylogeneticposition of Heronimus mollis (Digenea): evidence from 18S ribosomalRNA. Int. J. Parasitol. 23, 533–536.Bayssade-Dufour, C., Hugot, J.P., Albaret, J.L., 1993. Analyse phénétiquedes Microphalloidea (Trematoda) d’après la chétotaxie des cercaires.Syst. Parasitol. 25, 1–24.Blair, D., Barker, S.C., 1993. Affinities of the Gyliauchenidae: utility of the18S rRNA gene for phylogenetic inference in the Digenea (Platyhelminthes).Int. J. Parasitol. 23, 527–532.Blair, D., Bray, R.A., Barker, S.C., 1998. Molecules and morphology inphylogenetic studies of the Hemiuroidea (Digenea: Trematoda:Platyhelminthes). Mol. Phylogenet. Evol. 9, 15–25.Bray, R.A., 1987. A revision of the family Zoogonidae Odhner, 1902(Platyhelminthes: Digenea): subfamily Lepidophyllinae and commentson some aspects of biology. Syst. Parasitol. 9, 83–123.Bray, R.A., 1988. A discussion of the status of the subfamily BaccigerinaeYamaguti, 1958 (Digenea) and the constitution of the familyFellodistomidae Nicoll, 1909. Syst. Parasitol. 11, 97–112.Bray, R.A., 2002. Superfamily Gymnophalloidea Odhner, 1905. In: Gibson,D.I., Jones, A., Bray, R.A. (Eds.), Keys to the Trematoda, vol. 1. CABIPublishing and The Natural History Museum, Wallingford, pp.243–244.Bray, R.A., Cribb, T.H., 2001. A review of the family EnenteridaeYamaguti, 1958 (Digenea), with descriptions of species from Australianwaters, including Koseiria huxleyi n. sp. Syst. Parasitol. 48, 1–29.Bray, R.A., Cribb, T.H., Barker, S.C., 1996. Cableia pudica n. sp.(Digenea: Acanthocolpidae) from monacanthid fishes of the southernGreat Barrier Reef, Australia. Parasite 3, 49–54.Bray, R.A., Gibson, D.I., Zhang, J.-Y., 1999. Urotrematidae (Platyhelminthes:Digenea) in Chinese freshwater fishes. Syst. Parasitol. 44,193–200.Brooks, D.R., Bandoni, S.M., Macdonald, C.A., O’Grady, R.T., 1989.Aspects of the phylogeny of the Trematoda Rudolphi, 1808 (Platyhelminthes:Cercomeria). Can. J. Zool. 67, 2609–2624.Brooks, D.R., O’Grady, R.T., Glen, D.R., 1985. Phylogenetic analysis ofthe Digenea (Platyhelminthes: Cercomeria) with comments on theiradaptive radiation. Can. J. Zool. 63, 411–443.Brooks, D.R., Pérez-Ponce de León, G., León-Régàgnon, V., 2000.Phylogenetic analysis of the Enenteridae (Digenea, Lepocreadiidae)
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