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      Collyricloides massanae (Digenea, Collyriclidae): spermatozoon ultrastructure and phylogenetic importance Translated title: Collyricloides massanae (Digenea, Collyriclidae) : ultrastructure du spermatozoïde et importance phylogénétique

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          Abstract

          The spermatological characteristics of Collyricloides massanae (Digenea: Collyriclidae), a parasite of Apodemus sylvaticus caught in France, were studied by means of transmission electron microscopy. The mature sperm of C. massanae presents two axonemes of different lengths with the 9 + “1” pattern of the Trepaxonemata, two bundles of parallel cortical microtubules, external ornamentation of the plasma membrane, spine-like bodies, one mitochondrion, a nucleus and granules of glycogen. An analysis of spermatological organisation emphasised some differences between the mature spermatozoon of C. massanae and those reported in the Gorgoderoidea species studied to date, specially belonging to the families Dicrocoeliidae, Paragonimidae and Troglotrematidae. The ultrastructural criteria described in C. massanae such as the morphology of both anterior and posterior spermatozoon extremities, the association “external ornamentation + cortical microtubules”, the type 2 of external ornamentation and the spine-like bodies would allow us to bring closer the Collyriclidae to Microphalloidea. However, further ultrastructural and molecular studies are needed particularly in the unexplored taxa in order to fully resolve the phylogenetic position of the Collyriclidae.

          Translated abstract

          Les caractères spermatologiques de Collyricloides massanae (Digenea : Collyriclidae) parasite d’ Apodemus sylvaticus capturé en France, sont étudiés au microscope électronique à transmission. Le spermatozoïde mûr de C. massanae présente deux axonèmes de longueurs distinctes et de type 9 + « 1 » des Trepaxonemata, deux champs de microtubules corticaux parallèles, des ornementations externes, des corps épineux, une mitochondrie, un noyau et des granules de glycogène. Une analyse de l’organisation du spermatozoïde montre certaines différences entre le spermatozoïde mûr de C. massanae et ceux des espèces de Gorgoderoidea étudiées jusqu’ici, particulièrement celles appartenant aux familles Dicrocoeliidae, Paragonimidae et Troglotrematidae. Les critères ultrastructuraux décrits chez C. massanae tels que la morphologie des extrémités antérieure et postérieure, l’association « ornementation externe + microtubules corticaux », l’ornementation externe de type 2 et les corps épineux pourraient nous permettre de rapprocher les Collyriclidae des Microphalloidea. Cependant, des études ultrastructurales et moléculaires seront nécessaires, en particulier chez les taxa inexplorés, pour la résolution complète de la position systématique des Collyriclidae.

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          Most cited references 33

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          Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda).

          Complete small subunit ribosomal RNA gene (ssrDNA) and partial (D1-D3) large subunit ribosomal RNA gene (lsrDNA) sequences were used to estimate the phylogeny of the Digenea via maximum parsimony and Bayesian inference. Here we contribute 80 new ssrDNA and 124 new lsrDNA sequences. Fully complementary data sets of the two genes were assembled from newly generated and previously published sequences and comprised 163 digenean taxa representing 77 nominal families and seven aspidogastrean outgroup taxa representing three families. Analyses were conducted on the genes independently as well as combined and separate analyses including only the higher plagiorchiidan taxa were performed using a reduced-taxon alignment including additional characters that could not be otherwise unambiguously aligned. The combined data analyses yielded the most strongly supported results and differences between the two methods of analysis were primarily in their degree of resolution. The Bayesian analysis including all taxa and characters, and incorporating a model of nucleotide substitution (general-time-reversible with among-site rate heterogeneity), was considered the best estimate of the phylogeny and was used to evaluate their classification and evolution. In broad terms, the Digenea forms a dichotomy that is split between a lineage leading to the Brachylaimoidea, Diplostomoidea and Schistosomatoidea (collectively the Diplostomida nomen novum (nom. nov.)) and the remainder of the Digenea (the Plagiorchiida), in which the Bivesiculata nom. nov. and Transversotremata nom. nov. form the two most basal lineages, followed by the Hemiurata. The remainder of the Plagiorchiida forms a large number of independent lineages leading to the crown clade Xiphidiata nom. nov. that comprises the Allocreadioidea, Gorgoderoidea, Microphalloidea and Plagiorchioidea, which are united by the presence of a penetrating stylet in their cercariae. Although a majority of families and to a lesser degree, superfamilies are supported as currently defined, the traditional divisions of the Echinostomida, Plagiorchiida and Strigeida were found to comprise non-natural assemblages. Therefore, the membership of established higher taxa are emended, new taxa erected and a revised, phylogenetically based classification proposed and discussed in light of ontogeny, morphology and taxonomic history.
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            Infective larvae of Cercopithifilaria spp. (Nematoda: Onchocercidae) from hard ticks (Ixodidae) recovered from the Japanese serow (Bovidae)

            Hard ticks taken from the Japanese serow, Capricornis crispus, in Yamagata Prefecture, Honshu, harboured infective larvae of onchocercid filariae after incubation from the 22nd to the 158th day. Haemaphysalis flava and H. japonica contained one to eight filarial larvae; females, males and a nymph of the ticks were infected. The 44 infective larvae recovered were 612–1,370 μm long, and 11 of them, 930–1,340 μm long, were studied in detail. The larvae possessed the morphologic characteristics of the larvae of the genus Cercopithifilaria, namely an oesophagus with a posterior glandular part, no buccal capsule and a long tail with three terminal lappets. Five types (A to E) of infective larvae were identified based on the morphologic characteristics. While to date five species of Cercopithifilaria have been described from the Japanese serow, a specific identification of the larvae found in this study was generally not possible. Only type E larvae could be tentatively assigned to Cercopithifilaria tumidicervicata, as they had a cervical swelling similar to that of the adults of this species. A key for the identification of the five larval types is presented. The study presents circumstantial evidences indicating that H. flava and H. japonica may transmit Cercopithifilaria spp. to Japanese serows. It also suggests the possibility that such filarial larvae will be found in hard ticks anywhere, because Cercopithifilaria is distributed worldwide, though this genus generally goes unnoticed, as its microfilariae occur in the skin, not in the blood, of host animals.
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              Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies.

              New data on spermiogenesis and the ultrastructure of spermatozoa of 'true' tapeworms (Eucestoda) are summarized. Since 2001, more than 50 species belonging to most orders of the Eucestoda have been studied or reinvestigated, particularly members of the Caryophyllidea, Spathebothriidea, Diphyllobothriidea, Bothriocephalidea, Trypanorhyncha, Tetraphyllidea, Proteocephalidea, and Cyclophyllidea. A new classification of spermatozoa of eucestodes into seven basic types is proposed and a key to their identification is given. For the first time, a phylogenetic tree inferred from spermatological characters is provided. New information obtained in the last decade has made it possible to fill numerous gaps in the character data matrix, enabling us to carry out a more reliable analysis of the evolution of ultrastructural characters of sperm and spermiogenesis in eucestodes. The tree is broadly congruent with those based on morphological and molecular data, indicating that convergent evolution of sperm characters in cestodes may not be as common as in other invertebrate taxa. The main gaps in the current knowledge of spermatological characters are mapped and topics for future research are outlined, with special emphasis on those characters that might provide additional information about the evolution of tapeworms and their spermatozoa. Future studies should be focused on representatives of those major groups (families and orders) in which molecular data indicate paraphyly or polyphyly (e.g. 'Tetraphyllidea' and Trypanorhyncha) and on those that have a key phylogenetic position among eucestodes (e.g. Diphyllidea, 'Tetraphyllidea', Lecanicephalidea, Nippotaeniidea).
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                Author and article information

                Journal
                Parasite
                Parasite
                parasite
                Parasite
                EDP Sciences
                1252-607X
                1776-1042
                2014
                14 November 2014
                : 21
                : ( publisher-idID: parasite/2014/01 )
                Affiliations
                [1 ] CNRS – University of Corsica, UMR SPE 6134, SERME “Service d’Étude et de Recherche en Microscopie Électronique” 20250 Corte France
                [2 ] Laboratory of Evolutionary Biology, Ecology and Management of Ecosystems, Faculty of Sciences and Techniques, Cheikh Anta Diop University of Dakar BP 5055 Dakar Senegal
                [3 ] Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona Av. Joan XXIII, sn 08028 Barcelona Spain
                [4 ] Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona Av. Diagonal 645 08028 Barcelona Spain
                Author notes
                [* ]Corresponding author: quilichini@ 123456univ-corse.fr
                Article
                parasite140098 10.1051/parasite/2014061
                10.1051/parasite/2014061
                4230190
                25394323
                © A.J. Bakhoum et al., published by EDP Sciences, 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 56, Pages: 12
                Categories
                Research Article

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