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Phd Thesis SIMION 2014 THESE DE DOCTORAT DE L'UNIVERSITE PIERRE ET MARIE CURIE – PARIS VI École Doctorale 515 « Complexité du Vivant » Présentée pour obtenir le grade de Docteur de l'Université Pierre et Marie Curie par Paul SIMION Les cténophores : de leur position dans l'arbre des métazoaires (approche phylogénomique) à leur diversité taxonomique (phylogénie moléculaire et anatomie comparée) Soutenance prévue le 27 novembre 2014 Devant le jury composé de : Maximilian TELFORD, Professeur, University College London Rapporteur Didier CASANE, Professeur, Université Paris VII Rapporteur Evelyn HOULISTON, Directrice de Recherche CNRS Nicole BOURY-ESNAULT, Directrice de Recherche CNRS honoraire Frédéric DELSUC, Chargé de recherche CNRS Michaël MANUEL, Professeur, Université Paris VI Directeur de thèse Résumé Les cténophores représentent l’un des quatre embranchements animaux extérieurs aux Bilateria. La majorité des espèces sont planctoniques et gélatineuses, et sont reconnaissables à leurs huit rangées de peignes dont le battement permet la nage. Leur systématique est encore de nos jours mal comprise. L'anatomie des cténophores offre peu de caractères aussi bien pour placer la lignée dans l’arbre des métazoaires, que pour établir les relations de parenté au sein de l’embranchement et délimiter les espèces, et jusqu’à présent les données moléculaires n’ont pas permis de résoudre ces problèmes de manière satisfaisante. L’objectif de ce travail de thèse est de contribuer à améliorer notre compréhension de l'évolution des cténophores à différentes échelles taxonomiques. A l’échelle des métazoaires, la position phylogénétique des cténophores a été abordée par une approche phylogénomique. Un effort significatif a été réalisé pour améliorer l’échantillonnage taxonomique à travers le séquençage et l’assemblage des transcriptomes de 22 espèces de non-Bilateria (cténophores, cnidaires, spongiaires). Deux jeux de données indépendants ont été analysés, le premier représentant une mise à jour d’une supermatrice existante de 128 gènes ; le second (4235 gènes) ayant été entièrement construit de novo via un protocole original comportant la mise au point de nouvelles méthodes pour traiter de manière semi-automatisée les principales sources potentielles d’artéfact (contaminations, paralogies, données manquantes). Les résultats contredisent certaines études récentes en montrant que les spongiaires et non les cténophores représentent le groupe-frère des autres métazoaires. La position exacte de ces derniers reste à ce stade incertaine (trois options se présentant suivant les analyses). A l’échelle intra-phylétique, l'analyse d'un jeu de données comprenant les marqueurs ADNr 18S et Internal Transcribed Spacers (ITS), associée à des analyses de gènes dupliqués chez les cténophores et aux analyses phylogénomiques précédentes, a permis de résoudre une grande partie des relations phylogénétiques entre les ordres et les familles de cténophores, tout en permettant de préciser la position de la racine. Enfin, à une échelle taxonomique plus fine, une comparaison approfondie entre deux espèces du genre Pleurobrachia au moyen de marquages immunohistochimiques montre le potentiel de ces techniques comme source de nouveaux caractères structuraux « micro-anatomiques » à valeur diagnostique pour la délimitation et l’identification des espèces de cténophores. En conclusion, ce travail se veut une contribution au progrès de la systématique d’un embranchement encore méconnu et d’une grande importance pour la compréhension des évènements anciens de l’évolution animale. Abstract Ctenophores are one of the four animal phyla positioned outside from the Bilateria. Most ctenophore species are planktonic and gelatinous, and are easily recognisable by their eight comb rows used for swimming. Ctenophore systematics remains nowadays poorly understood. Anatomical characters do not help much in placing them within the animal tree, and similarly the grounds for establishment of their internal phylogeny as well as delimitation of species are notoriously weak due to a paucity of informative morpho-anatomical characters. Until now, the use of molecular data has failed to improve significantly this situation. The aim of this PhD thesis was to bring a contribution to our understanding of ctenophore evolution at different taxonomic scales. At the metazoan level, the position of ctenophores was addressed using a phylogenomic approach. Taxonomic sampling was significantly improved through sequencing and assembly of transcriptomes of 22 non-bilaterian species (belonging to ctenophores, cnidarians and sponges). Two independent datasets were analysed, one consisting in an update of an existing supermatrix of 128 genes, the other one (4235 genes) having been entirely built de novo, thanks to a newly-devised semi-automated protocol intended to eliminate all major potential causes of artefacts (contaminations, paralogies, missing data). Results clearly contradict recent phylogenomic studies which claimed Ctenophora to be the most early-diverging animal lineage, our analyses instead supporting Porifera as the sister-group to other metazoans. The exact position of ctenophores remains however uncertain at this stage, different conditions of analyses yielding three contradictory hypotheses as open possibilities. At the intra-phyletic level, analyses of a ADNr 18S and ITS (internal transcribed spacers) dataset, together with study of duplicated genes and the results of phylogenomic analyses, allowed resolving most phylogenetic relationships between ctenophore orders and families, including the placement of the ctenophore tree root. Finally, at smaller taxonomic scale, in-depth comparison between two species of the genus Pleurobrachia using immunohistochemistry demonstrates the potential of these techniques for uncovering new structural “micro-anatomical” characters useful for diagnosis and identification of ctenophore species. It is our hope that this work will contribute to improving the systematics of a poorly known phylum of great importance for understanding early animal evolution. Remerciements Mes plus profonds remerciements vont, évidemment, à Michaël, qui m©a inconditionnellement prêté sa confiance du début à la fin de cette thèse. Au-delà de ses (exceptionnelles) compétences scientifiques, je tiens à souligner ici ce qui est important : son admirable empathie. Attentif et présent, il a su détecter l©encadrement nécessaire à ma rigueur et la liberté nécessaire à mon humeur. C©était parfait. Mes remerciements les plus profonds (du coup, grosso modo à égalité avec Michaël¼) vont à Muriel, dont la bienveillance, l©énergie et la disponibilité forcent l©humilité. Elle m©a aidé aux moindres besoins, et il est difficile d©imaginer la montagne de difficultés que je n©ai jamais eu à affronter grâce à elle. Mais je la remercie surtout parce qu©elle géniale. Muriel, si vous la diluez dans l©eau, ça en fait dix normales. Je tiens à tout particulièrement remercier Hervé, d©abord pour son accompagnement tout au long de ces trois ans, ses conseils précieux et les biscuits bretons, mais également parce qu©en tant que responsable de l©école doctorale qui m©a accordé une bourse de thèse et président de mon comité de suivi, il a permis l©existence de ces recherches. Il pourra trouver dans ce manuscrit tous les arbres que j©ai trop tardé à lui montrer, je les lui doit bien ! Je remercie également, et chaleureusement, Éric pour son accompagnement durant cette thèse, ses discussions éclairées, ses questionnements stimulants, sa critique salutaire, et notre haine commune des imprimantes. Les conversations avec lui sont aussi intéressantes et variées que la Clairette de Die qu©il ramène est bonne. Je veux transmettre à Alicia, Karen, Joao et Thomas, tous mes remerciements du fond du cúur, à la fois pour les foultitudes de coups de mains dont ils m©ont fait l©honneur, mais surtout pour m©avoir continuellement accompagné dans la joie et la tendresse. Je tiens à leur dire tout le bonheur qu©ils m©apportent tous les jours depuis bientôt trois ans. Tous les jours, sans exception. Je remercie chaleureusement tous les membres du laboratoire, et du A4 en général, avec des mentions spéciales pour les membres de l©équipe AIRE, dont l©aide m©a été précieuse, et à Dominique, Philippe et Danielle pour leur soutien administratif. Je remercie également Muriel Umbhauer et Elisabeth Clément de l©école doctorale 515 pour leur aide, et enfin je remercie bien sûr Gaëlle Boutin dont la sympathie et la compétence surpassent mes défauts administratifs, c©est dire. Merci à Hervé Philippe et à Gert Wörheide, qui m©ont donné l©occasion de travailler avec eux, de profiter de leurs savoirs et de leur expérience. Merci de m©avoir accueilli dans vos laboratoires, ces voyages ont été pour moi extrêmement enrichissants. Merci également à Tetyana Nosenko bien sûr, ma toute première professeur de bio-informatique. Je remercie également Alexander Ereskovsky et Frédéric Delsuc pour leur accompagnement durant ma thèse, leur participation à mon comité de suivi et les différents services qu©ils n©ont jamais hésité à me rendre. Un grand merci à Evelyn Houliston et Olivier Gros pour leur accueil dans leurs laboratoires respectifs, et bien entendu merci aussi à Pascal, Carine, Tsuyoshi et Antonella. Je remercie également les pêcheurs de la station biologique de Villefranche-sur-Mer pour les petits tours en bâteau, et les membres de l©association de plongée Eden à Port-Louis pour les magnifiques ballades sous-marines. Je tiens à remercier aussi les « anciens jeunes », Cyrielle,
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