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Sex-Chromosome Evolution of Palearctic Tree Frogs in Space and Time

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Sex-Chromosome Evolution of Palearctic Tree Frogs in Space and Time Unicentre CH-1015 Lausanne http://serval.unil.ch Year : 2015 Sex-chromosome evolution of Palearctic tree frogs in space and time Dufresnes Christophe Dufresnes Christophe, 2015, Sex-chromosome evolution of Palearctic tree frogs in space and time 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_1F84E46189071 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’écologie et évolution Sex-chromosome evolution of Palearctic tree frogs in space and time Thèse de doctorat ès sciences de la vie (PhD) présentée à la Faculté de biologie et de médecine de l’Université de Lausanne par Christophe Dufresnes Biologiste diplômé de l’Université Joseph Fourrier de Grenoble Jury Prof. Vladimir Katanaev, Président Prof. Nicolas Perrin, Directeur de thèse Prof. John Pannell, expert Prof. Laurent Excoffier, expert Lausanne 201 5 3 TABLE OF CONTENTS Summar Résumé y . 5 Introduction . 6 Classical. model. .of . sex-chromosome. evolution. 7 Alternative models and implications . 7 Turnovers of sex chromosomes . 9 The evolution of XY recombination 9 Homomorphic sex chromosomes . and. .speciation . 10 Phylogeographic view of sex-chromosome evolution . 10 Model system: Palearctic tree frogs . 11 Chapters overview . 12 . 13 Part 1: Evolution of sex chromosomes in Hyla arborea Chapter I: Conservation phylogeography: does historical diversity contribute to regional vulnerability in European tree frogs (Hyla arborea)? Chapter II: Range-wide sex-chromosome sequence similarity supports . 16 occasional XY recombination in European tree frogs (Hyla arborea) Chapter III: Sex-chromosome differentiation parallels postglacial range . 33 expansion in European tree frogs (Hyla arborea ) . 38 Part 2: Evolution of sex chromosomes in Palearctic tree frogs Chapter IV: Cryptic diversity among Western Palearctic tree frogs: Postglacial range expansion, range limits, and secondary contacts of three European tree frog lineages (Hyla arborea group) Chapter V: Trans-species variation in Dmrt1 is associated . with. .sex . 52 determination in four European tree-frog species Chapter VI: Turnovers of ever-young sex chromosomes. in. .Palearctic . 62 tree frogs . 72 4 Chapter VII: Strong between-male variation of XY recombination in Hyla tree frogs . 94 Part 3: Homomorphic sex chromosomes and speciation Chapter VIII: Stronger transferability but lower variability in transcriptomic- than in anonymous microsatellites: evidence from Hylid frogs Chapter IX : .First-generation . linkage. map. .for . the. .European . .tree . frog. 101 (Hyla arborea) with utility in congeneric species Chapter X: Large-X effects despite sex-chromosome. homomorphy. 112 in European tree frogs . 118 Conclusions and perspectives . The evolution of XY recombination . 136 The ynamics of sex-chromosome turnovers . 136 Homomorphicd sex chromosomes and speciation. 138 Implications for conservation . 139 . 139 Appendix: Homologous sex chromosomes in three deeply-divergent anuran species . 141 References Acknowledgements . 149 Publication list . 155 . 157 Curriculum Vitae . 160 5 SUMMARY Sexual reproduction is nearly universal in eukaryotes and genetic determination of sex prevails among animals. The astonishing diversity of sex-determining systems and sex chromosomes is yet bewildering. Some taxonomic groups possess conserved and dimorphic sex chromosomes, involving a functional copy (e.g. mammals’ X, birds’ Z) and a degenerated copy (mammals’ Y, birds’ W), implying that sex- chromosomes are expected to decay. In contrast, others like amphibians, reptiles and fishes yet maintained undifferentiated sex chromosomes. Why such different evolutionary trajectories? In this thesis, we empirically test and characterize the main hypotheses proposed to prevent the genetic decay of sex chromosomes, namely occasional X-Y recombination and frequent sex-chromosome transitions, using the Palearctic radiation of Hyla tree frogs as a model system. We take a phylogeographic and phylogenetic approach to relate sex-chromosome recombination, differentiation, and transitions in a spatial and temporal framework. By reconstructing the recent evolutionary history of the widespread European tree frog H. arborea, we showed that sex chromosomes can recombine in males, preventing their differentiation, a situation that potentially evolves rapidly. At the scale of the entire radiation, X-Y recombination combines with frequent transitions to prevent sex-chromosome degeneration in Hyla: we traced several turnovers of sex-determining system within the last 10My. These rapid changes seem less random than usually assumed: we gathered evidences that one chromosome pair is a sex expert, carrying genes with key role in animal sex determination, and which probably specialized through frequent reuse as a sex chromosome in Hyla and other amphibians. Finally, we took advantage of secondary contact zones between closely-related Hyla lineages to evaluate the consequences of sex chromosome homomorphy on the genetics of speciation. In comparison with other systems, the evolution of sex chromosomes in Hyla emphasized the existence of consistent evolutionary patterns within the chaotic diversity of flexibility of cold-blooded vertebrates’ sex-determining systems, and provides insights into the evolution of recombination. Beyond sex-chromosome evolution, this work also significantly contributed to speciation, phylogeography and applied conservation research. 6 RÉSUMÉ La reproduction sexuée est quasi-universelle chez les eucaryotes et le sexe est le plus souvent déterminé génétiquement au sein du règne animal. L’incroyable diversité des systèmes de reproduction et des chromosomes sexuels est particulièrement étonnante. Certains groupes taxonomiques possèdent des chromosomes sexuels dimorphiques et très conservés, avec une copie entièrement fonctionnelle (ex : le X des mammifères, le Z des oiseaux) et une copie dégénérée (ex : le Y des mammifères, le W des oiseaux), suggérant que les chromosomes sexuels sont voués à se détériorer. Cependant les chromosomes sexuels d’autres groupes tels que les amphibiens, les reptiles et les poissons sont pour la plupart indifférenciés. Comment expliquer des trajectoires évolutives si différentes? Au cours de cette thèse, nous avons étudié empiriquement les processus évolutifs pouvant maintenir les chromosomes sexuels intacts, à savoir la recombinaison X-Y occasionnel ainsi que les substitutions fréquentes de chromosomes sexuels, en utilisant les rainettes Paléarctiques du genre Hyla comme modèle d’étude. Nous avons adopté une approche phylogéographique et phylogénétique pour appréhender les événements de recombinaison, de différenciation et de transitions de chromosomes sexuels dans un contexte spatio-temporel. En retraçant l’histoire évolutive récente de la rainette verte H. arborea, nous avons mis en évidence que les chromosomes sexuels pouvaient recombiner chez les mâles, empêchant ainsi leur différenciation, et que ce processus avait le potentiel d’évoluer très rapidement. A l’échelle plus globale de la radiation, il apparait que les phénomènes de recombinaison X-Y soient également accompagnés de substitutions de chromosomes sexuels, et participent de concert au maintien de chromosomes sexuels intacts dans les populations: le système de détermination du sexe des rainettes a changé plusieurs fois au cours des 10 derniers millions d’années. Ces transitions fréquentes ne semblent pas aléatoires: nous avons identifié une paire de chromosomes qui présente des caractéristiques présageant d’une spécialisation dans le déterminisme du sexe (notamment car elle possède des gènes importants pour cette fonction), et qui a été réutilisée plusieurs fois comme tel chez les rainettes ainsi que d’autres amphibiens. Enfin, nous avons étudié l’hybridation entre différentes espèces dans leurs zones de contact, afin d’évaluer si l’absence de différenciation entre X et Y jouaient un rôle dans les processus génétiques de spéciation. Outre son intérêt pour la compréhension de l’évolution des chromosomes sexuels, ce travail contribue de manière significative à d’autres domaines de recherche tels que la spéciation, la phylogéographie, ainsi que la biologie de la conservation. 7 INTRODUCTION Sexual reproduction is one of the best success- (reviewed by
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