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Sexual Selection and the Evolution of Female Ornaments: an Examination

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Sexual Selection and the Evolution of Female Ornaments: an Examination Sexual selection and the evolution of female ornaments : an examination of female plumage colouration using comparative analyses and long-term data sets collected in blue tit (Cyanistes caeruleus) populations Amélie Fargevieille To cite this version: Amélie Fargevieille. Sexual selection and the evolution of female ornaments : an examination of female plumage colouration using comparative analyses and long-term data sets collected in blue tit (Cyanistes caeruleus) populations. Animal biology. Université Montpellier, 2016. English. NNT : 2016MONTT127. tel-01647685 HAL Id: tel-01647685 https://tel.archives-ouvertes.fr/tel-01647685 Submitted on 24 Nov 2017 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. Délivré par l’Université de Montpellier Préparée au sein de l’école doctorale GAIA Et de l’unité de recherche « Centre d’Ecologie Fonctionnelle et Evolutive » à Montpellier Spécialité : Écologie, Évolution, Ressources Génétiques, Paléobiologie Présentée par Amélie FARGEVIEILLE Sélection sexuelle et évolution des ornements femelles Une étude d e la coloration du plumage femelle utilisant des analyses comparatives et des jeux de données à long terme issus de populations de mésange bleue ( Cyanistes caeruleus ). Soutenue le 13 décembre 2016 devant le jury composé de Dr. Claire DOUTRELANT, CR CNRS, CEFE Montpellier Directeur de thèse Dr. Arnaud GRÉGOIRE, MCF Université de Montpellier Co-directeur de thèse Dr. Hanna KOKKO, Professeur, University of Zurich Rapporteur Dr. Blandine DOLIGEZ, CR CNRS, LBBE Lyon Rapporteur Dr. Christophe THÉBAUD, Professeur, Université Paul Sabatier Examinateur Dr. Pierre-André CROCHET, DR CNRS, CEFE Montpellier Examinateur TABLE OF CONTENTS PARTIE FRANÇAISE (RÉSUMÉ ) 1 1. Approche interspécifique 8 2. Approche intraspécifique 12 CHAPTER 1 – INTRODUCTION 19 1. Traits implied in mate acquisition: historical view and sexual dimorphism 21 1.1. Sexual, social selection and secondary sexual characters 21 1.2. Asymmetric investment in reproduction and sexual dimorphism 22 1.3. Variation in sexual dimorphism 24 2. Origins and limits of female ornaments 26 2.1. Genetic correlation 26 2.2. Male mate choice, mutual mate choice 27 2.3. Female-female competition: intra-sexual selection and social selection 31 2.4. Alternative hypotheses 32 2.5. Limits of female ornamentation 33 3. Sexual/social selection in the wild: the necessity to consider spatiotemporal variation 34 4. For a better understanding of female ornamentation: the case of female plumage colouration 36 4.1. At the interspecific level 36 4.2. At the intraspecific level 38 5. Thesis main axes 40 INSERT 1: PLUMAGE COLOURATION AND ITS QUANTIFICATION 43 1. Chemical and physical colourations of plumage 43 2. Quantifying colourations 45 CHAPTER II – INTERSPECIFIC LEVEL 49 MS1 51 INSERT 2: THE BLUE TIT (CYANISTES CAERULEUS ) AS A SPECIES MODEL 81 1. Information regarding species and populations 81 2. Functions of blue tit colouration: what do we know 83 CHAPTER III – INTRASPECIFIC LEVEL 85 A - Assessing conditions leading to the evolution of colouration PART 1: Extracts from MS A1 87 MS2 95 MS3 123 B – Assortative mating on two coloured patches 141 MS4 141 MS5 183 CHAPTER IV – DISCUSSION 221 1. The interspecific level 223 1.1. Phenotypic and genetic correlation 224 1.2. Male investment in parental care and costs of reproduction 225 1.3. Breeding density 227 1.4. Further analyses 228 2. The intraspecific level 230 2.1. Spatiotemporal variation 230 2.2. The evolution of female colouration in blue tits 231 2.3. Further perspectives on selection 234 3. Conclusion 235 REFERENCES 237 ACKNOWLEDGEMENTS 257 APPENDIX 261 MS A1 263 PARTIE FRANÇAISE (RESUME) TABLE OF CONTENTS 1. Approche interspécifique 8 2. Approche intraspécifique 12 PARTIE FRANÇAISE Pour qu’ il y ait un changement évolutif par sélection chez une espèce, il faut que certains individus soient avantagés de manière à être capables de transmettre leurs caractères à leur descendance (Darwin 1871). Les traits associés au changement évolutif doivent être variables au sein de l’espèce, certaines valeurs de traits doivent avantager celui qui les porte et les niveaux d’expression (variation) des traits doivent être transmissibles à leur descendance. Au sein d’une espèce, certains individus peuvent être avantagés dans une propension particulière - l’accès à la reproduction - et par ce biais produire plus de descendance. Les traits qui leur donnent cet avantage sont sélectionnés par le processus de sélection sexuelle (Darwin 1871). Ces traits sont traditionnellement nommés caractères sexuels secondaires. La plupart des caractères sexuels secondaires sont associés aux mâles des espèces animales. Les travaux de Bateman (1948) et Trivers (1972) ont permis d’avancer une théorie expliquant la présence plus marquée des caractères sexuels secondaires chez les mâles. Leurs concepts se basent sur l’anisogamie, c’est -à-dire l’asymétrie dans la production des gamètes entre mâles et femelles. Les femelles produisent un faible nombre de gros gamètes et investissent dans les soins parentaux afin de maximiser les chances de survie de leurs descendants. D’un autre côté, les mâles produisent un grand nombre de gamètes de petite taille et maximisent le nombre de leurs descendants en multipliant les évènements de reproduction. Le nombre réduit de gamètes et l’investissement dans les soins parentaux par les femelles limitent leur possibilité de se reproduire avec de nombreux partenaires. Les femelles deviennent ainsi le sexe limitant et ont intérêt à choisir un bon partenaire afin de maximiser les chances de survie de leurs descendants. De leur côté les mâles entrent en compétition pour avoir accès aux femelles. Par cette vision, les caractères sexuels secondaires sont attendus comme plus développés chez les mâles qui sont limités dans leur accès à la reproduction. Il existe deux formes de compétition et de caractères sexuels secondaires associés. Les mâles peuvent entrer en compétition entre eux par le biais de combats ou en arborant des traits qui signalent leur dominance. On parle alors d’armements ou de badges de statut et de sélection intra-sexuelle. Ces armements ou badges de statut peuvent parfois permettre d’éviter des combats co ûteux en indiquant le niveau de dominance des individus qui les possèdent. Les mâles peuvent aussi être en compétition par leur attractivité auprès des femelles. Dans ce cas-là, on parle d’ornements arborés par les mâles et qui peuvent être préférés par les femelles par le biais de la sélection intersexuelle. Si les ornements sont répandus chez les mâles, il existe également de nombreuses espèces chez lesquelles les femelles peuvent aussi arborer des ornements, armements ou - 3 - PARTIE FRANÇAISE badges de statut. Historiquement les chercheurs, tel Darwin, avaient noté la présence de tels traits chez les femelles mais leur attention s’était portée sur le développement d’ un cadre théorique pour expliquer l’extravagance marqué e des traits mâles, extravagance qui constituait en elle-même un bon paradoxe évolutif. Lorsque les idées de Darwin furent reprises entre les années 1980 à 2000, les chercheurs s’intéressèrent également à tester empiriquement et théoriquement l’évolution d es ornements chez les mâles, notamment chez des espèces où la compétition pour l’accès aux femelles est très forte (espèces polygynes, espèces à système de lek) et présentant ce qui est appelé un fort dimorphisme sexuel (différence entre les sexes pour la valeur d’un trait ou de plusieurs traits). L’absence de dimorphisme sexuel, appelé monomorphisme, a été par contraste souvent reliée aux espèces monogames à soins biparentaux. L’hypothèse alors majoritairement acceptée pour expliquer la présence d’ornements chez les femelles était reliée au principe de corrélation génétique. Lande (1980) par le biais d’un modèle théorique a expliqué ce principe de la sorte : le caractère ancestral de l’espèce est monomorphique avec absence de traits ornementaux. Par le processus de sélection sexuelle, des traits ornementaux évoluent en premier lieu chez les mâles. Ils évoluent par la suite chez les femelles par le partage du matériel génétique transmis aux générations suivantes. Comme les femelles investissent plus dans la reproduction, ont leur fitness plus associée au nombre de descendants produits, peuvent être plus vulnérables à la prédation quand elles sont gravides, incubent ou s’occupent seules des jeunes , le processus de sélection naturelle réduit la valeur des traits ornementaux portés par les femelles. Dans le cas d’espèces monogames à soins biparentaux, une compétition réduite chez les mâles du fait d’une variance dans l’accès aux femelle s plus faible devrait entraîner une plus faible évolution des traits ornementaux chez les mâles et ces espèces devraient garder un monomorphisme sans traits extravagants. Aussi comme les mâles s’occup ent des descendants, leur survie pendant la phrase de soins parentaux est essentielle à la production de descendants et tout trait diminuant la vulnérabilité à la prédation pendant cette phase peut être favorisé.
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