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      Intermediate hosts of Protostrongylus pulmonalis (Frölich, 1802) and P. oryctolagi Baboš, 1955 under natural conditions in France

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          Abstract

          Background

          Protostrongylus oryctolagi and P. pulmonalis are causative agents of pulmonary protostrongyliasis in Lagomorphs in France. These nematodes need usually one intermediate host for its life cycle, a terrestrial snail. However, some studies, mainly in experimental conditions, have identified the species of snails acting as intermediate hosts.

          Methods

          In total, 3315 terrestrial snails and 307 slugs were collected in the field in South-Eastern France and analyzed to detect the presence of parasites. Identification of nematode parasites and snails were performed according to morphological and molecular approaches (D2 domain of the 28S rDNA for parasites; 18S and ITS-1 rDNA, COI and 16S mtDNA for snails).

          Results

          Eighteen snails were found positive for Protostrongylids larvae. Haplotypes of the larvae corresponding to sequences of P. oryctolagi and P. pulmonalis were detected. Morphological identification of molluscs based on shell characters revealed 4 different morphotypes, and molecular results confirm the membership of these gastropods to the Hygromiidae and revealed 4 different species: Candidula gigaxii, 2 species of Cernuella sp. and Xeropicta derbentina. All infested snails were collected in wine cultures.

          Conclusion

          This study displays the first description of intermediate hosts of P. oryctolagi and the first report of X. derbentina as natural intermediate host of P. pulmonalis.

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          Most cited references 80

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          Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships

          Background Reconstructing the higher relationships of pulmonate gastropods has been difficult. The use of morphology is problematic due to high homoplasy. Molecular studies have suffered from low taxon sampling. Forty-eight complete mitochondrial genomes are available for gastropods, ten of which are pulmonates. Here are presented the new complete mitochondrial genomes of the ten following species of pulmonates: Salinator rhamphidia (Amphiboloidea); Auriculinella bidentata, Myosotella myosotis, Ovatella vulcani, and Pedipes pedipes (Ellobiidae); Peronia peronii (Onchidiidae); Siphonaria gigas (Siphonariidae); Succinea putris (Stylommatophora); Trimusculus reticulatus (Trimusculidae); and Rhopalocaulis grandidieri (Veronicellidae). Also, 94 new pulmonate-specific primers across the entire mitochondrial genome are provided, which were designed for amplifying entire mitochondrial genomes through short reactions and closing gaps after shotgun sequencing. Results The structural features of the 10 new mitochondrial genomes are provided. All genomes share similar gene orders. Phylogenetic analyses were performed including the 10 new genomes and 17 genomes from Genbank (outgroups, opisthobranchs, and other pulmonates). Bayesian Inference and Maximum Likelihood analyses, based on the concatenated amino-acid sequences of the 13 protein-coding genes, produced the same topology. The pulmonates are paraphyletic and basal to the opisthobranchs that are monophyletic at the tip of the tree. Siphonaria, traditionally regarded as a basal pulmonate, is nested within opisthobranchs. Pyramidella, traditionally regarded as a basal (non-euthyneuran) heterobranch, is nested within pulmonates. Several hypotheses are rejected, such as the Systellommatophora, Geophila, and Eupulmonata. The Ellobiidae is polyphyletic, but the false limpet Trimusculus reticulatus is closely related to some ellobiids. Conclusions Despite recent efforts for increasing the taxon sampling in euthyneuran (opisthobranchs and pulmonates) molecular phylogenies, several of the deeper nodes are still uncertain, because of low support values as well as some incongruence between analyses based on complete mitochondrial genomes and those based on individual genes (18S, 28S, 16S, CO1). Additional complete genomes are needed for pulmonates (especially for Williamia, Otina, and Smeagol), as well as basal heterobranchs closely related to euthyneurans. Increasing the number of markers for gastropod (and more broadly mollusk) phylogenetics also is necessary in order to resolve some of the deeper nodes -although clearly not an easy task. Step by step, however, new relationships are being unveiled, such as the close relationships between the false limpet Trimusculus and ellobiids, the nesting of pyramidelloids within pulmonates, and the close relationships of Siphonaria to sacoglossan opisthobranchs. The additional genomes presented here show that some species share an identical mitochondrial gene order due to convergence.
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            Nematode Parasites of Vertebrates: Their Development and Transmission

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              A phylogeny of the land snails (Gastropoda: Pulmonata).

              We have undertaken the first large-scale molecular phylogenetic analysis of the Stylommatophora. Sequences of the ribosomal RNA gene-cluster were examined in 104 species of snails and slugs from 50 families, encompassing all the currently recognized major groups. It allows an independent test of the present classification based on morphology. At the level of families our molecular phylogeny closely supports the current taxonomy, but the deep branches within the tree do not. Surprisingly, a single assemblage including the families Achatinidae, Subulinidae and Streptaxidae lies near the base of the tree, forming a sister group to all remaining stylommatophorans. This primary division into 'achatinoid' and 'non-achatinoid' taxa is unexpected, and demands a radical reinterpretation of early stylommatophoran evolution. In particular, the Orthurethra appear to be relatively advanced within the 'non-achatinoid clade', and broadly equivalent to other super-familial clusters. This indicates that supposedly primitive features such as the orthurethran kidney are derived. The molecular tree also suggests that the origin of the Stylommatophora is much earlier than the main period of their diversification.
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                Author and article information

                Contributors
                lesage.celia@gmail.com
                cecile.patrelle@gmail.com
                vrignaud.sylvain@free.fr
                anouk.decors@oncfs.gouv.fr
                hubert.ferte@univ-reims.fr
                damien.jouet@univ-reims.fr
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                15 February 2015
                15 February 2015
                2015
                : 8
                Affiliations
                [ ]EA 4688 (VECPAR), UFR de Pharmacie, Université de Reims Champagne-Ardenne, 51 rue Cognacq-Jay, 51096 Reims, France
                [ ]Office National de la Chasse et de la Faune Sauvage, Direction des études et de la recherche, 5 rue de Saint Thibaud, 78610 Auffargis, France
                [ ]USR 3278 CNRS-EPHE-Université Perpignan, Perpignan, France
                Article
                717
                10.1186/s13071-015-0717-5
                4336746
                © Lesage et al.; licensee BioMed Central. 2015

                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 credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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