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The Role of Bat Flies (Nycteribiidae) in the Ecology and Evolution of the Blood Parasite Polychromophilus (Apicomplexa: Haemosporida)

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The Role of Bat Flies (Nycteribiidae) in the Ecology and Evolution of the Blood Parasite Polychromophilus (Apicomplexa: Haemosporida) Unicentre CH-1015 Lausanne http://serval.unil.ch Year : 2014 THE ROLE OF BAT FLIES (NYCTERIBIIDAE) IN THE ECOLOGY AND EVOLUTION OF THE BLOOD PARASITE POLYCHROMOPHILUS (APICOMPLEXA: HAEMOSPORIDA) WITSENBURG Fardo WITSENBURG Fardo, 2014, THE ROLE OF BAT FLIES (NYCTERIBIIDAE) IN THE ECOLOGY AND EVOLUTION OF THE BLOOD PARASITE POLYCHROMOPHILUS (APICOMPLEXA: HAEMOSPORIDA) Originally published at : Thesis, University of Lausanne Posted at the University of Lausanne Open Archive http://serval.unil.ch Document URN : urn:nbn:ch:serval-BIB_AEE221052C906 Droits d’auteur L'Université de Lausanne attire expressément l'attention des utilisateurs sur le fait que tous les documents publiés dans l'Archive SERVAL sont protégés par le droit d'auteur, conformément à la loi fédérale sur le droit d'auteur et les droits voisins (LDA). A ce titre, il est indispensable d'obtenir le consentement préalable de l'auteur et/ou de l’éditeur avant toute utilisation d'une oeuvre ou d'une partie d'une oeuvre ne relevant pas d'une utilisation à des fins personnelles au sens de la LDA (art. 19, al. 1 lettre a). A défaut, tout contrevenant s'expose aux sanctions prévues par cette loi. Nous déclinons toute responsabilité en la matière. Copyright The University of Lausanne expressly draws the attention of users to the fact that all documents published in the SERVAL Archive are protected by copyright in accordance with federal law on copyright and similar rights (LDA). Accordingly it is indispensable to obtain prior consent from the author and/or publisher before any use of a work or part of a work for purposes other than personal use within the meaning of LDA (art. 19, para. 1 letter a). Failure to do so will expose offenders to the sanctions laid down by this law. We accept no liability in this respect. Département d’Ecologie et d’Evolution THE ROLE OF BAT FLIES (NYCTERIBIIDAE) IN THE ECOLOGY AND EVOLUTION OF THE BLOOD PARASITE POLYCHROMOPHILUS (APICOMPLEXA: HAEMOSPORIDA) Thèse de doctorat ès sciences de la vie (PhD) présentée à la Faculté de biologie et de médecine de l’Université de Lausanne par Fardo WITSENBURG Master en Evolutionary Biology de l’Université de Groningen. Jury Prof. Grégoire Millet, Président Dr. Philippe Christe, Directeur de thèse Dr. Karen McCoy, expert Prof. Nadir Alvarez, expert Lausanne 2014 voor Opa en Oma, die me hebben moeten missen ACKNOWLEDGEMENTS This thesis is the product of four and a half years of work. But more than that, it is the product of many people who have made sure that this period, and consequently this thesis, has been a success. First, and foremost I would like to thank Philippe, my supervisor. I am already thankful just for the fact that he hired me, replying to my failed attempt to get a scholarship, but I am especially grateful to him for, from the beginning onwards, trusting me and my project. Unlike myself, I have never caught him doubting the directions I was proposing and supported me in what I was doing. It is truly amazing to have enjoyed this confidence trough out this period, and for that I say thanks. Secondly I would like to thank my exam-committee: Karen McCoy, Nadir Alvarez and Grégoire Millet, for your constructive, enthusiastic and overall friendly support. I would also like to thank here my two committee-members-turned-fruitful-collaborators: Nicolas Salamin and Jérôme Goudet. Three other pleasant collaborations were with Laura Clément, Franzi Schneider and Ludo Dutoit, my three master students. I am eternally grateful for the work they have contributed to this thesis and for being cool people overall. I would like to thank Igor Pavlinić, Jorge Palmeirim, Adrià López- Baucells, Martin Ševčík, Dino Scaravelli and Mikael Paillet. It is amazing how one can email complete strangers with the request to disturb their local bat populations and that they not only happily comply, but all turn out to be great characters. The barbecue at the shores of Lac Léman will continuously be on offer and I hope I may see you all once again. My gratitude goes to the loosely banded groupe Christe. First of all I would like to thank Tania. She injected the team with very much appreaciated and contagious enthusiasm, both scientific and personal. And she was my B&B. Jess, merci pour chaleureusement ridiculiser mon français. Juan was the best company in the office, basically abolishing the need for breaks. Fabrice, thanks for our super scientific discussions, despite the lack of white board. And Céline, both my travail au labo and mon écriture would not have been the same without you. i Next are people who may not be part of any study, but supplied me with many tips, tricks and spelling or, if even not that, at least were awesome enough to make me come to work in the first place. Jess, Alan, Katie, Valentijn, Dumas, Emma, Laetitia, Ivan, Miguel, Manuel, Sophie, Olivier, Rike, Christine, José, Ricardo, Mikko, Sylvain, Reto, Roberto, Céline, Marie, Simon, Erica, Mathias, Sayaka, Pawel, Marta & Martha. Many of the above have also been kind enough to help in the middle of the night capturing, bleeding and feeding bats. Wow. In particular a big thank you for Nadia, who was a godsend and could show and explain me all chiropteran practicalities. For the lab- crew, a particular, grand merci for Catherine and Anne-Lyse who were always willing to give advice on all things molecular. Lastly, much appreciation goes to Isa & Christophe for the meals, and Elisa & Alberto for the bed. Generally, this department is full of wonderful people. From off-campus I have to mention ‘les Pichardiens’. Merci pour me donner à Lausanne une maison chaleureuse, drôle, aventuristique et sucré & salé. In particular I would like to give a big hug to Nadine, who let me in, and changed life forever. My Dutch friends, thanks for staying so close, where ever. My parents, I send you my greatest gratitude for having always accepted, supported and even stimulated my excursions and enterprises even though you’d rather just have me on the couch in your kitchen. Joris and Franzi, I just want to mention you here because you’re awesome. Thanks for dropping by and being there. Finally I would like to thank Beat. For having made work, and especially life in general, seem wonderful. ii RÉSUMÉ La coévolution est l’évolution réciproque de deux organismes en interaction. Au sein d’une association hôte-parasite, ce sont ces interactions qui modèlent l’histoire de vie du parasite. Les parasites hétéroxènes requièrent deux hôtes pour compléter leur cycle de vie. Un fameux exemple de parasite hétéroxène est celui des parasites responsables de la malaria qui requièrent un vecteur diptère et un hôte vertébré. L’écologie évolutive des parasites responsables de la malaria est de ce fait déterminée par la biologie de l’hôte ainsi que celle du vecteur et peut être vue comme le produit de l’évolution d’une interaction triple. Polychromophilus spp. (Apicomplexa: Haemosporidae) sont des parasites responsables de la malaria qui utilisent de manière spécifique les chauves-souris comme hôte vertébré, et sont transmis par un ectoparasite, la nyctéribie (Diptera: Nycteribiidae). Cette thèse décrit l’écologie et l’évolution de Polychromophilus spp. et comment leur coévolution avec les nyctéribies a modelé ces processus. Pour trouver l’origine évolutive de Polychromophilus, j’ai construit une analyse phylogénétique de l’Ordre des Haemosporidae, basée sur trois gènes. Polychromophilus est placé près de la base du clade des Plasmodium de sauropsidés. Cela suggère que Polychromophilus représente un second et indépendant évènement d’invasion des mammifères par un parasite Haemosporidae. Le changement de vecteur pour les Nycteribiidae a dû se produire après la spécialisation du parasite pour les chauves- souris. La dispersion d’un parasite hétéroxène est supposée dépendre uniquement de son hôte le plus mobile. En utilisant des analyses microsatellites, je démontre que le vecteur nyctéribie a un niveau de dispersion à travers l’Europe supérieur à l’hôte chauve-souris. Cependant, après comparaison des distances génétiques par paire de l’ADN mitochondrial, ni le vecteur ni l’hôte ne corrèlent significativement avec le parasite. De ce fait, la structure de population d’un parasite transmis par un vecteur ne reflète pas simplement la structure de population de son hôte le plus mobile. La iii distribution d’haplotypes du parasite suggère plutôt des effets fondateurs du parasite, un haut renouvellement des parasites ou une hétérogénéité du taux de dispersion des hôtes. Les comportements et dynamiques du parasite, du vecteur et de l’hôte au sein d’une seule population sont déterminés par diverses interactions entre les trois acteurs. Des expériences de choix d’hôte et de survie montrent que les nyctéribies augmentent leur survie en se nourrissant préférentiellement sur des chauves-souris dont la parasitémie est plus faible. Néanmoins, la distribution naturelle des vecteurs au sein des hôtes est indépendante de la parasitémie de ces derniers. Bien que l’infection par Polychromophilus est liée à de plus faibles conditions corporelles chez les chauves–souris adultes, les effets pathologiques de l’infection restent méconnus, peut-être parce que les plus lourdes infections se retrouvent chez les jeunes. Cette thèse démontre comment les Nycteribiidae influencent l’écologie évolutive de Polychromophilus. Cependant, la complexité des niveaux d’interaction, non seulement entre le parasite et ses deux hôtes, mais aussi entre les chauves-souris et leurs ectoparasites rendent difficile les prédictions sur l’épidémiologie de ce parasite. iv SUMMARY Coevolution is the reciprocal evolution of two interacting organisms. In a parasite-host association it is these interactions that shape the life history of the parasite. Heteroxenous parasites require two hosts to complete their life cycle.
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