Sex Expression and the Selection and Évolution of Combined Sexes in the Dioecious Annual Herb Mercurialis Annua

Unicentre CH-1015 Lausanne http://serval.unil.ch RRRRYear : 2017 Sex expression and the selection and évolution of combined sexes in the dioecious annual herb Mercurialis annua Cossard Guillaume Cossard Guillaume, 2017, Sex expression and the selection and évolution of combined sexes in the dioecious annual herb Mercurialis annua 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_7B6611EE0BD10 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). 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Département d’Ecologie et d’Evolution Sex expression and the selection and evolution of combined sexes in the dioecious annual herb Mercurialis annua Thèse de doctorat ès sciences de la vie (PhD) présentée à la Faculté de biologie et de médecine de l’Université de Lausanne par Guillaume COSSARD Biologiste diplômé de l’Université de Rennes1, Jury Prof. Medhi Tafti, Président Prof. John R. Pannell, Directeur de thèse Prof. Gabriel Marais, expert Prof. Tadeusz J. Kawecki, expert Lausanne 2017 Acknowledgments I would like first to thank John for supervising my thesis work during the last five years, with invariable interest for the work I was doing. I consider him a great scientist from whom I took inspiration many times during my Ph.D. I especially thank him for is capacity to look at alternative hypothesis, and always be willing to approach results from different angles to throw the most light on them. I have been interested in plant biology for a long time, and John gave me the opportunity to extend this passion when he accepted me as a student. Finally, he put such great effort into supervising my work and helping me with interpreting and writing up its results that this thesis would have never been possible without his help and advice. Many members of the Pannell lab have provided help for this thesis work, without which I would have never been able to gather the amount of data I needed for my analysis. Especially I would like to thank: Luis Santos del Blanco, Xinji Li, Jörn Gerchen, Thomas Martignier, Paris Veltsos, Melissa Toups, Cindy Dupuis, Imane El M'Ghari, Felix Gréverath, Ana Paula Machado, Loic Liberati, Sébastien Tesson, Rachidos, Melvyn Staiff, Clément Jaulin, Camille Roux, Aline Revel and Yves Cuénot. A special thanks goes to the two technicians whose help and skills have not only been of great help for my work, but also an incredible source of learning in domains that were not my specialty before I arrived in Lausanne. First, there is Nicolas Ruch, in charge of plant cultures, who dedicated so much time to the maintenance of our plants, curing them when they desperately needed it, recovering them from the bad conditions to which I sometimes subjected them, and designing setups to allow my experiments to take place. It has been a pleasure to work with him in the greenhouses during the years of my thesis research. Second, I would not have been able to conduct much of the laboratory work without the help and guidance of Dessislava Savova Bianchi, who has always been incredibly patient and willing to help in any circumstances with my lab work. I would also like to thank the students I accompanied and who helped me with setting up experiments and collecting data: Laure Olazcuaga, Yi Huang and Katerina Hanuzova. Finally, I thank all those with whom I shared so many great moments, friends I met in Switzerland who share with me many sweet memories. They are too many to cite here, but I am sure they will recognize themselves if they ever come to read these lines. 1 2 Abstract The flowering plants display a large variety of sexual systems that has long astonished botanists. The great majority of species are hermaphroditic, carrying male and female organs within the same flower, while others are characterized by sexes separated between different individuals, a system termed dioecy. The later is likely to have evolved from the ancestral state of hermaphroditism and had long been considered an evolutionary dead-end. However recent progress in our understanding of transitions between sexual systems in plants has shed light on frequent transitions away from dioecy, arguing against the evolutionary dead-end hypothesis. The determinants of transitions towards dioecy likely involve an intermediate step of either gynodioecy (where females coexist with hermaphrodites) or monoecy (where individuals carry unisexual flowers of both sexes). The principle aim of this thesis was to investigate factors that may lead dioecious species towards a state of combined sexes, either hermaphroditism or monoecy. My investigation builds on seminal work conducted by the evolutionary theorist David Lloyd in the 1970s, who observed the often labile nature of sex expression in dioecious populations, where females and males may sometimes produce pollen or seeds, respectively. Lloyd proposed that this ‘inconstancy’ or ‘leakiness’ in sex expression constitutes variation on which natural selection can act to bring about the breakdown of dioecy and the evolution of combined sexes. To investigate this idea, I studied populations of Mercurialis annua, a dioecious herb growing in Europe and around the Mediterranean Basin and that is characterized by the presence of lability in sex expression. My goals were to assess how males and females differ, both in their patterns of inconstancy and the underlying gene expression profiles, and to determine the functionality of this inconstancy in natural dioecious populations. I found that most of the inconstant reproductive effort of both males and females had a negligible effect on fitness in natural conditions. However, I reasoned that when plants are isolated from large populations, inconstant individuals should enjoy a strong advantage by being able to reproduce by selfing. Because I detected that females were more frequently inconstant than males in natural populations, I hypothesized that females should benefit more from isolation. I tested this hypothesis by removing males from experimental populations of dioecious M. annua and allowing the remaining females to evolve in their absence. These females showed a dramatic increase in pollen production over four generations, with a large proportion of the male-less populations being functionally hermaphroditic. I also investigated how the profiles of sex expression in the evolved individuals had shifted, and found that most of the genes that were originally more highly expressed in males than females to be up-regulated as well in the selected females. Together, my results show that inconstancy is a trait underlined by genetic variation on which selection may act during episodes of isolation, and can indeed provide a starting point for transitions away from dioecy. 3 4 Résumé La grande diversité de systèmes sexuels qui présentent les plantes à fleurs à depuis longtemps intrigué les botanistes. La grande majorité des espèces sont hermaphrodites, portant les organes mâles et femelles au sein de la même fleur, tandis qu’une minorité se caractérise par la séparation des sexes entre différents individus, un système appelé dioécie. Ce-dernier a probablement évolué à partir de l’état ancestral hermaphrodite et a longtemps été considéré comme une impasse évolutive. Cependant de récentes avancées dans notre compréhension de l’évolution des transitions entre systèmes sexuels chez les plantes semblent indiquer que la dioécie peut évoluer vers des systèmes où les sexes sont combinés, contredisant l’hypothèse de l’impasse évolutive. Les déterminants des transitions vers la dioécie impliquent sûrement des étapes intermédiaires de gynodioécie (où femelles et hermaphrodites coexistent) ou de monoécie (où les individus portent des fleurs unisexuelles des deux sexes). Le but principal de cette thèse est d’étudier les facteurs qui peuvent amener une espèce dioïque a transiter vers un état de sexes combinés, soit l’hermaphroditisme, soit la monoécie. Mon étude se base sur le travail fondateur du théoricien David Lloyd dans les années 1970, qui a observé que la nature souvent labile de l’expression du sexe dans les populations dioïques, où les femelles et les mâles parfois produisent du pollen et des graines, respectivement. Lloyd a proposé que cette ‘inconstance’ dans l’expression du sexe pourrait constituer un variation sur laquelle la sélection pourrait agir et déclencher une rupture de la dioécie et l’évolution d’un système où les sexes sont combinés. Afin d’explorer cette idée, j’ai étudié les populations de Mercurialis annua, une herbe dioïque présente en Europe et autour du bassin méditerranéen, caractérisée par la présence d’inconstance de l’expression du sexe.

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