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The Nematoda Filarioidea: Critical Analysis Linking Molecular and Traditional Approaches Bain O.*, Casiraghi M.**, Martin C.* & Uni S.***

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The Nematoda Filarioidea: Critical Analysis Linking Molecular and Traditional Approaches Bain O.*, Casiraghi M.**, Martin C.* & Uni S.*** Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2008153342 THE NEMATODA FILARIOIDEA: CRITICAL ANALYSIS LINKING MOLECULAR AND TRADITIONAL APPROACHES BAIN O.*, CASIRAGHI M.**, MARTIN C.* & UNI S.*** Summary: The traditional tool includes the morphological cha- The molecular analysis of the Filarioidea and the endobacteria racters of the adult and larval phenotypes, the biolo- Wolbachia is no more limited to the agents of human diseases gical data provided by vectors and experimental rodent and the diversified sampling permits a synthesis with the models of filariases, as well as the host range and geo- morphological and biological results. The validity of the genera with “uncoherent host range”, such as Mansonella, Litomosoides graphical distribution of worms. Since Wehr (1935), and Cercopithifilaria, is confirmed and, consequently, their several classifications have been built on these data and evolution by host-switchings. Dirofilaria and Onchocerca, types of the most recent (Anderson & Bain, 1976), seemed to two subfamilies, appear more closely related than with other provide a correct synthesis; however new features, onchocercids. Waltonellinae from anurans and Oswaldofilariinae from reptiles have a basal position. These filariae, and some such as the discovery of genera or the better know- others also considered primitive, do not harbour Wolbachia. ledge of larval development, have revealed several pro- Evidence for transversal transmission of the bacteria and a second blems. acquisition event is given with the supergroup F, identified in Nowadays, molecular analyses are available for a rather Mansonella, in one of the Cercopithifilaria species and in arthropods. important sample of filariae, including also the study of the endosymbionts Wolbachia sensu lato (Casiraghi KEY WORDS : Filarioidea, Onchocerca, Dirofilaria, Dipetalonema, Wolbachia, phylogeny. group and collaborators, work in progress). The genes studied are 5S rDNA, 12S rDNA and coxI, less often 18S rDNA. Our aim is to compare the results of both approaches ilarioids are parasitic nematodes extensively stu- with some examples chosen to distinctly highlight died because several species are the agents of confirmation or contradiction of previous interpretations, Fhuman diseases. The need to elucidate the epide- and finally to delineate some unresolved problems. miological conditions of transmission and the require- ment for relevant experimental models have stimulated a widespread zoological investigation. Our present EXAMPLES OF CONGRUENCE concern is the systematics of the superfamily Filarioidea with emphasis on its generic composition, the relation- BETWEEN MOLECULAR ships between genera, the validity of the supra-generic AND TRADITIONAL ANALYSES divisions, the roots and epoch of emergence of Fila- rioidea, related to the question of mono- or polyphyly. mong the filariae, there are several genera of Two main investigative tools are currently available, the which the host range is “zoologically incohe- traditional morphological and biological, and the more Arent” (Chabaud, 1981, see Chabaud & Bain, recent molecular analyses. They are commonly used 1994). They are used to argue a model of evolution by independent specialized teams, with the risk of through host-switchings (captures), in opposition to a uncontrolled divergent interpretations for the same parallel evolution of the hosts and their parasites. biological object. On the other hand, the combining However it may be objected that the genus is not well- of their respective results may foster more appropriate delineated and, in fact, is a non-natural grouping of interpretations. species. The molecular analyses should decipher such artefacts. * Parasitologie Comparée et Modèles Expérimentaux, USM 307, The congruence of the two methods of analyses appears Muséum National d’Histoire Naturelle, 75231 Paris Cedex 05, France. quite good for the three genera studied Cercopithifi- ** Dipartimento di Biotecnologie e Bioscienze, Università degli Studi laria Eberhard, 1980, Litomosoides Chandler, 1931 and di Milano Bicocca, Piazza della Scienza 2, 20126 Milano, Italy. Mansonella Faust 1929, parasitic in mammals. *** Department of Medical Zoology, Osaka City University Medical School, Osaka 545-8585, Japan. Cercopithifilaria is known with 28 species described Correspondence: Odile Bain – E-mail: [email protected] from monkeys, ruminants, carnivores, lagomorphs, por- Parasite, 2008, 15, 342-348 342 Xth EMOP, August 2008 FILARIOIDEA, CRITICAL ANALYSIS cupine and murid rodents, marsupials and mono- observed in anthropoid and platyrhinian monkeys. tremes. The small subunit of mitochondrial ribosome Other hosts are insectivores, including tupaids, carni- (12S rRNA) was analysed for nine species, from African vores and sciurid and caviomorph rodents (Eberhard porcupine hystricid, Japanese bear, Japanese bovids & Orihel, 1984). Recently, ruminant ungulates have and cervids. The taxon, which had been created for a joined this large host-range with species initially assi- parasite of African cercopithecid monkeys, is actually gned to Cutifilaria Bain & Schulz-Key, 1974, now a a group of species having a large host-range and a subgenus of Mansonella. The 5S rDNA and/or 12S worldwide distribution. As a matter of fact, the 12S rDNA analyses (Xie et al., 1994; work in progress) have rDNA analysis confirms the value of the traditional cha- been performed with one species of Cutifilaria and racters used to define Cercopithifilaria (Fig. 1), the three species from primates belonging to the subge- adult morphology and the infective larvae with no or nera Mansonella, Esslingeria Chabaud & Bain, 1976 minute buccal cavity. In addition adults have dermal and Tetrapetalonema Faust, 1935, respectively. They or sub-cutaneous localizations, and skin-dwelling micro- cluster together and this correlates with distinctive filariae. The vectors are the hard ticks Rhipicephalidae morphological characters in adult worms: the oeso- and it is hypothesized that they had the major role in phagus is thread-like, its blurred anterior end fused the spread and diversification of Cercopithifilaria. In with the muscular body layer, and no buccal capsule Australia, C. johnstoni Spratt & Varughese, 1975, type is identifiable (Fig. 1). Wolbachia was not detected in host-Muridae, is found in marsupials and monotremes M. (E.) perstans (Grobusch et al., 2003) but was detec- as well (communication by D. Spratt) and this might ted in the other three species; it belongs to the super- represent the first step of future speciations. Interes- group F of the endosymbiont (work in progress). tingly, Wolbachia is absent from species of the genus, except C. japonica (Uni, 1983) from bears, which har- bours the form F of the endosymbiont (work in pro- gress), a Wolbachia type shared with filariae of the IS THE DIPETALOMEMA LINEAGE A REALITY? genus Mansonella and with some arthropod hosts (Casi- raghi et al., 2005). uring the past 30 years, Dipetalonema Diesing, 32 species have been described in Litomosoides, from 1861 has been split into several subgenera, microchiropterans, marsupials, murids and a few other Dmany elevated to the generic rank, and the rodents. The 12S rRNA was analysed for five species, whole encompassed in the “Dipetalonema line”. A three from bats and two from murids. The monophyly common history from a Gondwanian ancestor during is also proved in this case. A particular morphological the late Second era was proposed for all of them, fol- character of the cluster is the large segmented buccal lowed by divergences in the different regions separated capsule, about 20 µm long in the adult worm and third by the continental drift (Chabaud & Bain, 1976, in Cha- stage larva (Fig. 1). The vectors are macronyssid aca- baud & Bain, 1994). In the “Dipetalonema line” males rians. Litomosoides is confined to the New World and display a basic arrangement of the caudal sensory has intensely diversified in the Neotropical region, system (four precloacal pairs, pairs 5 and 6 post-cloa- probably by means of the mites. In the Old World, cal, and a posterior group of pairs 7 to 10); the area another genus has a large segmented buccal capsule rugosa, a cuticular anti-slit apparatus used during and is parasitic in microchiropterans, and a common mating, is generally present. However the lineage is origin is supposed for the two genera. Indeed, a spe- composed of plesiomorph and derived species (such cies parasitc in North American rodents Geomyioidea, as Acanthocheilonema and Cercopithifilaria, respecti- Litomosa westi (Gardner & Schmidt, 1986), which was vely), and a clear definition was difficult. The present initially placed in Litomosoides, would represent a link. question is: do the molecular data support the Dipe- This hypothesis is supported by the 12S rDNA analysis talonema lineage? (Casiraghi et al., 2004; work in progress). Wolbachia Among its 17 genera and sub-genera, half of them have is present in Litomosoides, with one exception (L. yuta- been submitted to molecular analyses: Acanthocheilo- jensis Guerrero, Martin & Bain, 2003) and belongs to nema Cobbold 1870, Dipetalonema, Cercopithifilaria, the supergroup D; Wolbachia of Litomosa westi appears and Mansonella with four of its sub-genera, Manso- to belong to the same supergroup (work in progress). nella, Esslingeria Chabaud & Bain, 1976, Tetrapetalo- Mansonella Faust, 1929 contains 29 species, among nema Faust, 1935, and Cutifilaria. which three are human parasites: one
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