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Cooperation and Competition As Drivers of the Evolutionary Transition from Simultaneous Hermaphroditism to Separate Sexes in Ophryotrocha Worms Laura Picchi

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Cooperation and Competition As Drivers of the Evolutionary Transition from Simultaneous Hermaphroditism to Separate Sexes in Ophryotrocha Worms Laura Picchi Cooperation and competition as drivers of the evolutionary transition from simultaneous hermaphroditism to separate sexes in Ophryotrocha worms Laura Picchi To cite this version: Laura Picchi. Cooperation and competition as drivers of the evolutionary transition from simulta- neous hermaphroditism to separate sexes in Ophryotrocha worms. Invertebrate Zoology. Université Sorbonne Paris Cité, 2018. English. NNT : 2018USPCD025. tel-02464068 HAL Id: tel-02464068 https://tel.archives-ouvertes.fr/tel-02464068 Submitted on 2 Feb 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. UNIVERSITÉ PARIS 13 École doctorale Galilée Unité de recherche Laboratoire d’Éthologie Expérimentale et Comparée Thèse pour obtenir le grade de Docteur de l'Université Paris 13 Discipline Éthologie Présentée et soutenue publiquement par Laura PICCHI Le 18 décembre 2018 Titre : Cooperation and competition as drivers of the evolutionary transition from simultaneous hermaphroditism to separate sexes in Ophryotrocha worms. Directeur de thèse : Maria Cristina LORENZI Composition du jury Président du jury Patrizia D’ETTORRE professeure au LEEC, Université Paris 13 Rapporteurs Philippe JARNE DR au CEFE/CNRS Montpellier Stuart WEST professeur à l’ Oxford University Directeur de thèse M. Cristina LORENZI professeure au LEEC, Université Paris 13 “Despite the Victorians’ reputation for prudishness, nineteenth-century natural philosophers spent lots of time watching animals mate” J. Knight, in Sexual stereotypes, Nature (2002) Coopération et compétition comme éléments moteurs de la transition évolutive de l’hermaphrodisme vers des sexes sépares chez les vers du genre Ophryotrocha Résumé Chez les animaux, l’hermaphrodisme et le gonochorisme sont tous deux apparus plusieurs fois de manière indépendante. Cependant, les voies évolutives impliquées dans la transition entre les systèmes sexuels sont en grande partie inconnues. L’objectif de cette thèse était donc d’étudier la transition évolutive de l’hermaphroditisme vers des sexes séparés chez les vers du genre Ophryotrocha, en s'intéressant en particulier à la manière dont la coopération et la compétition entre individus peuvent déterminer l’allocation de ressources reproductives chez les hermaphrodites, soit en favorisant l'évolution de sexes séparés ou en stabilisant l'hermaphrodisme. Nos résultats ont révélé que les vers hermaphrodites échangent réciproquement des œufs, une forme de coopération qui favorise une allocation des ressources sexuelles biaisée en faveur de la fonction femelle et qui stabilise ainsi l'hermaphrodisme. Toutefois, lorsque les hermaphrodites sont exposés à une forte compétition pour l'accouplement, ils transfèrent les ressources de la fonction femelle vers la fonction mâle, ce qui diminue la production d'œufs et les soins parentaux, mais augmente la motilité et l'agressivité. À des niveaux élevés de compétition pour l'accouplement, motilité et agression peuvent améliorer la recherche et la monopolisation du partenaire, favorisant ainsi la propagation des hermaphrodites biaisés en faveur de la fonction mâle, promouvant ainsi l'évolution de mâles purs et, ensuite, de femelles pures. Enfin, nous avons montré que les hermaphrodites prêts à s'accoupler en tant que mâles uniquement (sans œufs matures) préfèrent des partenaires hermaphrodites prêts à s'accoupler en tant que femelles, qui, en revanche, n'expriment aucune préférence. Globalement, ce travail montre que la coopération et la compétition sont tous deux des facteurs importants dans la répartition des sexes chez les hermaphrodites et suggère que des changements dans l’environnement social ont pu jouer un rôle central dans l’évolution des systèmes sexuels chez les vers du genre Ophryotrocha. Mots clés : systèmes sexuels, compétition pour la reproduction, allocation sexuelle, polychètes Cooperation and competition as drivers of the evolutionary transition from simultaneous hermaphroditism to separate sexes in Ophryotrocha worms Abstract In animals, both simultaneous hermaphroditism and gonochorism originated independently several times. Yet the evolutionary pathways involved in the transition between sexual systems are largely unknown. The aim of this thesis is therefore to investigate the evolutionary transition from hermaphroditism to separate sexes in Ophryotrocha worms, focusing on how cooperation and competition between individuals shape hermaphrodite sex allocation, either promoting the evolution of separate sexes or stabilizing hermaphroditism. Our results revealed that hermaphroditic worms reciprocally exchange egg-clutches, a form of cooperation that favor a female-biased sex allocation and stabilizes hermaphroditism. However, when hermaphrodites are exposed to high level of mate competition, they reallocate resources from the female to the male function, decreasing egg production and parental care and increasing motility and aggression. Under high mate competition level, motility and aggression may improve mate searching and partner monopolization and may favor the spread of male-biased hermaphrodites, promoting the evolution of pure males and, later, pure females. Finally, we showed that hermaphrodites ready to mate as males only (without ripe eggs) prefer hermaphrodites ready to mate as females as partners, which, in contrast, do not express any preference. Overall, this work shows that both cooperation and competition are important factors in hermaphrodite sex allocation, and suggests that changes in the social environment may have played a central role in the evolution of sexual systems in Ophryotrocha worms. Key words: sexual systems, mate competition, sex allocation, polychaetes Laboratoire d’Éthologie Expérimentale et Comparée Université Paris 13 – 99, avenue J.-B. Clément – 93430 Villetaneuse – France Preface The chapters of this thesis constitute a set of papers in preparation for submission, submitted or published in peer-reviewed journals. Publications included in this thesis Book chapters Picchi L., Lorenzi M.C. (in press). Polychaete worms on the brink between hermaphroditism and separate sexes. In: Transitions between Sexual Systems (Leonard J.L. ed). Springer Verlag. Peer reviewed journals Picchi L., Cabanes G., Ricci-Bonot C., Lorenzi M.C. (2018). Quantitative matching of clutch size in reciprocating hermaphroditic worms. Current Biology in press. Santi M., Picchi L., Lorenzi M.C. (2018). Dynamic modulation of reproductive strategies in a simultaneous hermaphrodites and the preference for the male role. Animal Behaviour in press. Lorenzi M.C., Araguas A., Bocquet C., Picchi L., Ricci-Bonot C. 2018. Courtship as a war of attrition in a simultaneous hermaphrodite. Animal Biology in press. Talks at meetings Picchi, L., Perrin L., Maury C., Lorenzi M.C. Gender-related behaviours in hermaphrodites and the transition to separate sexes. SHOW: Simultaneously Hermaphroditic Organisms Workshop, Paris (France) 14-16 February March 2018. Picchi, L., Ricci-Bonot, C., Cabanes, G., Lorenzi M.C. Reciprocal Egg-trading in a simultaneous hermaphrodite. 14th International Congress on Invertebrate Reproduction and Development, Italy, 2017 (Napoli, 29-30 August, 2017 – Firenze, 1-2 September, 2017). Picchi, L., Ricci-Bonot, C., Lorenzi M.C. Egg reciprocation in a simultaneous hermaphrodite. Annual meeting of the Societé Francaise pour l'Etude du Comportement Animal SFECA. Gif-sur-Yvette, France, April 2017. Picchi, L., Ricci-Bonot C., Lorenzi M.C. Outcrossing hermaphrodites: solving the conflict through reciprocation. SHOW: Simultaneously Hermaphroditic Organisms Workshop, Lund (Sweden) 8-10 March 2017. Abstract Book p. 8. Posters at meetings Picchi L., Ricci-Bonot C., Cabanes, G., Lorenzi M.C. Dummies can do it: conditional egg reciprocation and numerical matching of egg clutches in pairs of polychaete worms. Evolution, II Joint Congress on Evolutionary Biology, Montpellier (France) 19 - 22 August 2018. Picchi L., Ricci-Bonot C., Lorenzi M.C. Parental care and reciprocal egg-exchange in a simultaneous hermaphrodite. International student meeting Ecology & Behaviour, Chizé (France) 19 - 23 June 2017. Meeting organization SHOW: Simultaneously Hermaphroditic Organisms Workshop, Paris (France) 14-16 February March 2018 (in collaboration with Céline Bocquet and Maria Cristina Lorenzi). Contents 1. Introduction ........................................................................................................................ 13 Sexual systems and William’s paradox ................................................................................ 14 Selective advantages of simultaneous hermaphroditism and gonochorism ......................... 18 Fisher’s condition and “extraordinary sex ratios”: the role of cooperation and competition in shaping sex allocation ........................................................................................................... 20 Sex allocation in simultaneous hermaphrodites ................................................................... 22 Evolutionary pathways from hermaphroditism to gonochorism and vice
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