Jean Mariaux

Phylogeny of the orders of the Eucestoda (Cercomeromorphae) based on comparative morphology : Historical perspectives and a new working hypothesis

The phylogeny of the Eucestoda was evaluated based on a suite of 49 binary and multistate characters derived from comparative morphological and ontogenetic studies; attributes of adult and larval tapeworms were considered. A single most parsimonious tree (MPT) (consistency index = 0.872; retention index = 0.838; and homoplasy index = 0.527) was fully resolved and is specified by the following: (Gyrocotylidea, (Amphilinidea, ((Spathebothriidea, (Pseudophyllidea, ((Diphyllidea, (Trypanorhyncha, (Tetraphyllidea, (Lecanicephalidea, ((Nippotaeniidea, (Tetrabothriidea, Cyclophyllidea)), Proteocephalidea))))), Haplobothriidea))), Caryophyllidea))). Monophyly for the Eucestoda was firmly corroborated. Trees derived from the primary and bootstrap analyses were congruent, but low values, particularly for relationships among the tetrafossate tapeworms, indicated additional examination is warranted. The MPT was found to be the most efficient hypothesis for describing character evolution and in specifying relationships among the orders when compared to those concepts that had been developed for the tapeworms over the past century. Areas of congruence were shared among the current hypothesis and one or more of the prior hypotheses. Major conclusions include: (1) Caryophyllidea are basal and monozooy is ancestral; (2) difossate forms are primitive, and the Pseudophyllidea are the sister group of the strongly polyzoic tapeworms; (3) Nippotaeniidea are highly derived; (4) the higher tapeworms (Tetraphyllidea, Lecanicephalidea, Proteocephalidea, Nippotaeniidea, Tetrabothriidea, and Cyclophyllidea) are closely related or potentially coordinate groups: (5) Tetrabothriidea and the Cyclophyllidea are sister groups; and (6) Tetraphyllidea is paraphyletic, with the Onchobothriidae basal to the Phyllobothriidae. Character support for placement of the Tetrabothriidea continues to be contradictory, and this order may represent a key to understanding the phylogeny of the higher cestodes. The current study constitutes a complete historical review and poses a new and robust hypothesis for the phylogeny of the Eucestoda.

Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences

The phylogenetic relationships and systematic position of the members of the suborder Plagiorchiata, one of the derived and most diverse groups of Digenea, have always been controversial. Here, we present a phylogeny of this group based on the analysis of partial sequences of the lsrDNA in 28 species representing 13 families of Plagiorchiata, as well as four outgroups. Our results show that the Plagiorchiata, as considered by most authors, is not monophyletic, and that the superfamilies Opecoeloidea, and most probably Dicrocoelioidea and Gorgoderoidea, may have to be removed from this suborder. According to our results, the Plagiorchiata includes only parasites of terrestrial vertebrates. We find the Plagiorchiata to be composed of two well-supported clades which can be ranked as superfamilies: (1) Plagiorchioidea, including the Plagiorchiidae, Haematoloechidae, Telorchiidae, Brachycoeliidae and Leptophallidae; and (2) Microphalloidea containing the Microphallidae, Prosthogonimidae, Lecithodendriidae and Pleurogenidae. The genetic analysis also allowed revision of the position of several taxa of Plagiorchiata, including: (1) a confirmation of the position of the Brachycoeliidae within the Plagiorchiata; (2) a close phylogenetic relationships of Macrodera with Paralepoderma, Leptophallus and Metaleptophallus; (3) the grouping of Opisthioglyphe and Telorchis within a distinct and strongly supported clade; and (4) the placement of Allassogonoporus amphoraeformis within the Pleurogenidae, and not close to Lecithodendriidae. Some systematic changes, corresponding to these results, are proposed.

Cestode systematics: Any progress?

In this short review, I summarize the recent advances, the present state and future for research in the field of cestode systematics. First, within an historical context, I briefly outline why our understanding of relationships within the Eucestoda has been problematic and contentious. On this foundation, I then summarize and discuss recent progress at various supraspecific levels, and at the specific level. Of particular interest in this respect is the discrepancy between the methods applied to understand the evolution of a few well-studied taxa, for instance the complex of Echinococcus species, contrasted with our relative ignorance about the systematic status of the vast majority of species. This leads to a review of the diversity of classical and new methodologies currently applied in the field of cestode systematics. Applications of morphoanatomical investigations as well as more recent molecular tools are examined, and some less common approaches are also reviewed. Finally, several practical and theoretical difficulties that are specific to the domain are discussed. These include problems in accessibility of material and adequate consideration of host-specificity. Our current state of knowledge represents an apparent paradox in that significant progress has indeed been achieved during the last 15 years, but appears limited to very specific cases, principally among medically important taxa. Conversely, more general works whose utility has been long recognized have not been addressed despite their conceptual simplicity. Consequently the development of new techniques, especially molecular ones, to allow access to new classes of characters is encouraged. However the need for continuous effort using more traditional approaches, including continued field collection, excellent and detailed descriptions and redescriptions, as well as critical revisions of classical monographs is also emphasized. A synergism linking morphological and molecular characters and phylogenetic approaches to analysis provides a firm foundation for rapid and seminal advances in the elucidation of relationships among the Eucestoda.

MOLECULAR SYSTEMATICS OF MESOCESTOIDES SPP. (CESTODA: MESOCESTOIDIDAE) FROM DOMESTIC DOGS (CANIS FAMILIARIS) AND COYOTES (CANIS LATRANS)

The genus Mesocestoides Vaillant, 1863 includes tapeworms of uncertain phylogenetic affinities and with poorly defined life histories. We previously documented 11 cases of peritoneal cestodiasis in dogs (Canis familiaris L.) in western North America caused by metacestodes of Mesocestoides spp. In the current study, DNA sequences were obtained from metacestodes collected from these dogs (n = 10), as well as proglottids from dogs (n = 3) and coyotes (Canis latrans Say, 1823 [n = 2]), and tetrathyridia representing laboratory isolates of M. corti (n = 3), and these data were analyzed phylogenetically. Two nuclear genetic markers, 18S ribosomal DNA and the second internal-transcribed spacer (ITS 2), were sequenced. Phylogenetic analysis of the 18S rDNA data recovered a monophyletic group composed of all samples of Mesocestoides spp., distinct from closely related outgroup taxa (Amurotaenia Akhmerov, 1941 and Tetrabothrius Rudolphi, 1819). Initial analysis of the ITS 2 data resolved 3 clades within Mesocestoides. Two proglottids from dogs formed a basal clade, a second clade was represented by tetrathyridial isolates, and a third clade included all other samples. Interpretation of these data from an apomorphy-based perspective identified 6 evolutionary lineages. We also assessed whether metacestodes from dogs (n = 4) are capable of asexual proliferation in laboratory mice. One tetrathyridial and 2 acephalic isolates from dogs proliferated asexually. Further investigation is warranted to determine which of the lineages represent distinct species and to determine the life history strategies of Mesocestoides spp.

Origin and evolution of African Polystoma (Monogenea: Polystomatidae) assessed by molecular methods ☆

Among Polystomatidae (Monogenea), the genus Polystoma, which mainly infests neobatrachian hosts, is the most diverse and occurs principally in Africa, from where half the species have been reported. Previous molecular phylogenetic studies have shown that this genus originated in South America, and later colonised Eurasia and Africa. No mention was made on dispersal corridors between Europe and Africa or of the origin of the African Polystoma radiation. Therefore, a molecular phylogeny was inferred from ITS1 sequences of 21 taxa comprising two species from America, seven representatives from Europe and 12 from Africa. The topology of the phylogenetic tree reveals that a single event of colonisation took place from Europe to Africa and that the putative host carrying along the ancestral polystome is to be found among ancestral pelobatids. Percentage divergences estimates suggest that some presumably distinct vesicular species in unrelated South African anurans and some neotenic forms found in several distinct hosts in Ivory Coast, could, in fact, belong to two single polystome species parasitising divergent hosts. Two main factors are identified that may explain the diversity of African polystomes: (i), we propose that following some degree of generalism, at least during the juvenile stages of both hosts and parasites, distinctive larval behaviour of polystomes engenders isolation between parasite populations that precludes sympatric speciations; (ii), cospeciation events between Ptychadena hosts and their parasites are another factor of diversification of Polystoma on the African continent. Finally, we discuss the systematic status of the Madagascan parasite Metapolystoma, as well as the colonisation of Madagascar by the host Ptychadena mascareniensis.

Nomimoscolex suspectus n. sp. (Eucestoda: Proteocephalidea: Zygobothriinae) with morphological and molecular phylogenetic analyses of the genus.

We describe a new species of Nomimoscolex from the Amazon siluriform fishes Brachyplatystoma filamentosum, B. flavicans and B. vaillanti. It differs from N. piraeeba in a lower mean number of testes, the paramuscular position of the vitelline follicles, the ovarian width/proglottis width ratio and the cirrus-pouch length/proglottis width ratio. Protein electrophoresis assays performed for 25 enzymatic systems showed that specimens of N. suspectus n. sp. from the three host species form a homogenous population which was genetically isolated from N. piraeeba and N. dorad. Moreover, the latter two species, synonymised by Rego (1991) because of their close morphological similarity, could be separated at eight loci. We thus restore N. dorad as a valid species. We finally examined the composition of the genus Nomimoscolex using DNA sequences from the 5.8S rRNA, ITS-2 and 28S rRNA nuclear ribosomal genes and a matrix of 24 morphological characters. Phylogenetic relationships were inferred for nine species of the genus, five members of other monticelliid genera and two outgroup species. The results of the phylogenetic analyses performed on morphological and molecular characters converged with those from allozyme studies and showed that N. suspectus, N. piraeeba and N. dorad clustered in a distinct clade that excluded other members of the genus. We therefore recognised them as an aggregate of species to reflect an isolation supported by both morphological and genetic data. Because relationships among the remaining Nomimoscolex representatives and other genera were generally poorly resolved, regardless of the database analysed, no action was taken to reorganise them into alternative groupings.

A New Genus and Species of Proteocephalidean (Cestoda) From Clarias Catfishes (Siluriformes: Clariidae) in Africa

Abstract A new proteocephalidean cestode is described from 2 catfishes, Clarias gariepinus (type host) and C. cf. anguillaris (Siluriformes: Clariidae), from Ethiopia (type locality), Sudan, Tanzania, and Zimbabwe, and a new genus, Barsonella, is proposed to accommodate it. The genus belongs to the Proteocephalinae because its genital organs (testes, ovary, vitellarium, and uterus) are situated in the medulla. Barsonella lafoni, the type and only species of the new genus, is characterized mainly by the possession of an additional opening of each sucker; circular musculature on the anterior margin of suckers, serving as a sphincter; a small thin-walled glandular apical organ; absence of well-developed osmoregulatory canals in mature, pregravid, and gravid proglottids; and a large strobila, up to 173 mm long and 3.2 mm wide. Species of Marsypocephalus Wedl, 1861 (Marsypocephalinae), other large-sized proteocephalidean tapeworms occurring sympatrically in African catfishes (Clarias and Heterobranchus) and also possessing a sphincter-like, circular musculature on the anterior part of suckers, differ from B. lafoni in the absence of an additional sucker opening and glandular apical organ, the cortical position of the testes, well-developed osmoregulatory canals throughout the strobila, and a large cirrus sac. Proteocephalus glanduligerus (Janicki, 1928), another cestode parasitic in Clarias spp. in Africa, is much smaller than B. lafoni (maximum length 15 mm), has suckers without additional opening and circular musculature on the suckers, a large-sized glandular organ, much larger than suckers, and well-developed osmoregulatory canals. Comparison of partial sequences of the 28S rRNA gene for 7 samples of B. lafoni from 2 different hosts and 4 localities in Ethiopia, Sudan, and Tanzania has shown a very low genetic variability. In a limited phylogenetic analysis, B. lafoni formed a clade with Corallobothrium solidum Fritsch, 1886 (Proteocephalidae: Corallobothriinae), an African electric catfish parasite. This clade was the sister group of almost all Neotropical taxa from pimelodid and other catfishes.

SANDONELLA SANDONI (LYNSDALE, 1960), AN ENIGMATIC AND MORPHOLOGICALLY UNIQUE CESTODE PARASITIC IN THE OSTEOGLOSSIFORM FISH HETEROTIS NILOTICUS IN AFRICA

Sandonella sandoni (Lynsdale, 1960) is the type and only species of the Sandonellinae, a cestode subfamily of unclear phylogenetic position. It is redescribed here on the basis of a re-examination of its syntypes, voucher specimens from museum collections, and freshly collected material from the intestine of Heterotis niloticus (Osteoglossiformes: Arapaimidae) from Benin, Nigeria, Senegal, and the Sudan. The species possesses several unique morphological characters, such as (1) a vitellarium formed by 2 compact, but deeply lobulated, postovarian masses near the posterior margin of proglottids; (2) a scolex with a highly modified apical structure formed by 4 muscular retractile lappets; (3) a well-developed circular musculature, which is external to the inner longitudinal muscles; (4) a dilated, vesicle-like proximal part of the external sperm duct; (5) the unique morphology of the uterus and its development, which represents an intermediate form between the 2 basic types recognized in the Proteocephalidea; (6) the growth of eggs during their development within the uterus; and (7) the complex proglottization with intermingled smaller and larger (wider) proglottids. The morphology of S. sandoni, including the form and distribution of microtriches, was studied by scanning electron microscopy for the first time, and the lectotype and paralectotypes of S. sandoni are designated. Sequences of the 28S rRNA gene of 4 specimens (2 from the Sudan and 2 from Senegal) were identical, which confirms conspecificity of geographically distant samples. Sandonella sandoni sequences have also shown that it actually belongs among the Proteocephalidea, being a sister taxon of a relatively derived clade of Palaearctic proteocephalideans, containing Glanitaenia osculata and Paraproteocephalus parasiluri from catfish and Palaearctic species of the Proteocephalus aggregate.

A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda)

Abstract Proteocephalidean tapeworms form a diverse group of parasites currently known from 315 valid species. Most of the diversity of adult proteocephalideans can be found in freshwater fishes (predominantly catfishes), a large proportion infects reptiles, but only a few infect amphibians, and a single species has been found to parasitize possums. Although they have a cosmopolitan distribution, a large proportion of taxa are exclusively found in South America. We analyzed the largest proteocephalidean cestode molecular dataset to date comprising more than 100 species (30 new), including representatives from 54 genera (80%) and all subfamilies, thus significantly improving upon previous works to develop a molecular phylogeny for the group. The Old World origin of proteocephalideans is confirmed, with their more recent expansion in South America. The earliest diverging lineages are composed of Acanthotaeniinae and Gangesiinae but most of the presently recognized subfamilies (and genera) appear not to be monophyletic; a deep systematic reorganization of the order is thus needed and the present subfamilial system should be abandoned. The main characters on which the classical systematics of the group has been built, such as scolex morphology or relative position of genital organs in relation to the longitudinal musculature, are of limited value, as demonstrated by the very weak support for morphologically-defined subfamilies. However, new characters, such as the pattern of uterus development, relative ovary size, and egg structure have been identified, which may be useful in defining phylogenetically well-supported subgroups. A strongly supported lineage infecting various snakes from a wide geographical distribution was found. Although several improvements over previous works regarding phylogenetic resolution and taxon coverage were achieved in this study, the major polytomy in our tree, composed largely of siluriform parasites from the Neotropics, remained unresolved and possibly reflects a rapid radiation. The genus Spasskyellina Freze, 1965 is resurrected for three species of Monticellia bearing spinitriches on the margins of their suckers.

Revision of Gangesia (Cestoda: Proteocephalidea) in the Indomalayan region: morphology, molecules and surface ultrastructure.

Tapeworms of Gangesia Woodland, 1924 (Cestoda: Proteocephalidea) parasitic in freshwater fishes in the Indomalayan Region were critically reviewed. Evaluation of type specimens and newly collected materials from Bangladesh, Cambodia and India, as well as critical examination of extensive literature have shown that only the following four species, instead of 48 nominal species of Gangesia and Silurotaenia Nybelin, 1942 reported from this region (36 new synonymies proposed), are valid: Gangesia bengalensis (Southwell, 1913), type-species of the genus and most common parasite of Wallago attu (Siluridae), G. macrones Woodland, 1924 typical of Sperata seenghala (Bagridae), both species characterized by the possession of two circles of hooks on the rostellum-like organ and several rows of hooklets on the anterior margins of suckers; G. agraensis Verma, 1928 from W. attu (typical host), which has the scolex with only one circle of hooks and 1–3 incomplete rows of tiny hooklets on the suckers; and G. vachai (Gupta and Parmar, 1988) n. comb. from several catfishes, which possesses 4–6 circles of hooks and 5–11 rows of hooklets on the anterior half of suckers. Scolex morphology, including surface ultrastructure (microtriches), of all but one species (G. vachai) is described for the first time using scanning electron microscopy. A phylogenetic analysis based on the partial sequences encoding the large nuclear ribosomal subunit RNA gene has shown that three Indomalayan species, namely G. bengalensis, G. macrones and G. vachai, form a monophyletic group within Gangesia, whereas G. agraensis tends to form a clade with the Palaearctic species of the genus. A table with differential characters of all species from the Indomalayan Region is also provided together with a key to identification of genera of the subfamily Gangesiinae. The present study demonstrates that species of Silurotaenia do not occur in the Indomalayan region.