Towards an adaptive and genomic understanding of an exaggerated secondary sexual trait in water striders William Toubiana To cite this version: William Toubiana. Towards an adaptive and genomic understanding of an exaggerated secondary sex- ual trait in water striders. Biodiversity. Université de Lyon, 2019. English. NNT : 2019LYSEN058. tel-02360159 HAL Id: tel-02360159 https://tel.archives-ouvertes.fr/tel-02360159 Submitted on 12 Nov 2019 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. Numéro National de Thèse : 2019LYSEN058 THESE de DOCTORAT DE L’UNIVERSITE DE LYON opérée par l’Ecole Normale Supérieure de Lyon Ecole Doctorale N° 340 Biologie Moléculaire, Intégrative et Cellulaire (BMIC) Discipline : Sciences de la vie Soutenue publiquement le 20/09/2019, par : William Toubiana Towards an adaptive and genomic understanding of an exaggerated secondary sexual trait in water striders Vers une compréhension adaptative et génomique d’un trait sexuel secondaire chez une espèce d’insecte semi-aquatique. Devant le jury composé de : Dr. Leulier François Group leader ENS de Lyon Examinateur Dr. Immonen Elina Group leader University of Uppsala Rapporteure Dr. Perry Jennifer Group leader University of Oxford Rapporteure Dr. Lüpold Stefan Group leader University of Zurich Examinateur Dr. Khila Abderrahman Group leader ENS de Lyon Directeur de thèse 1 2 Table of contents Abstract ................................................................................................................................................................... 6 Résumé .................................................................................................................................................................... 7 Introduction ............................................................................................................................................................. 9 I. The history of evolutionary thought ............................................................................................................. 9 II. The process of selection in evolution........................................................................................................ 12 A. Natural selection ................................................................................................................................... 12 B. Genetic drift .......................................................................................................................................... 13 III. The theory of sexual selection ................................................................................................................. 13 IV. Fitness ..................................................................................................................................................... 16 V. Sexual dimorphism ................................................................................................................................... 17 VI. Trait exaggeration ................................................................................................................................... 18 A. Trait exaggeration and sexual selection ................................................................................................ 18 B. Other types of trait exaggeration........................................................................................................... 19 VII. Evo-Devo of exaggerated sexually-selected traits ................................................................................. 21 A. Growth pathways and their role in variable and non-variable exaggerations ....................................... 22 B. The role of patterning genes in the development of exaggerated, sexually-selected traits ................... 23 VIII. Towards a more genomic understanding of trait exaggeration ............................................................. 23 IX. Intra-species variation in sexually selected traits .................................................................................... 25 X. The semiaquatic insects (Gerromorpha) as a model to study the role of natural and sexual selections on trait evolution .................................................................................................................................................... 26 Chapter 1: Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon .................................................................................................................................. 31 I. Abstract: ..................................................................................................................................................... 32 II. Introduction .............................................................................................................................................. 33 III. Material & methods ................................................................................................................................. 34 A. Population sampling and culture .......................................................................................................... 34 B. Measurement of Microvelia species and statistics ................................................................................ 34 C. Behavioral observations and video acquisition ..................................................................................... 35 D. Microvelia phylogenetic reconstruction ............................................................................................... 35 E. Male competition assay ......................................................................................................................... 35 F. Fight frequency assay ............................................................................................................................ 35 G. Artificial selection experiment ............................................................................................................. 36 H. Condition-dependence experiment ....................................................................................................... 36 I. Microsatellite development .................................................................................................................... 36 J. Paternity test .......................................................................................................................................... 37 IV. Results and discussion ............................................................................................................................. 37 3 A. Sexual Dimorphism and scaling relationships in Microvelia species ................................................... 37 B. Mating systems in Microvelia species. ................................................................................................. 39 C. Intensity of male competition in M. longipes compared to M. pulchella .............................................. 42 D. Effect of exaggerated leg length on male reproductive fitness in M. longipes ..................................... 43 E. Environmental and genetic contributions to male rear leg variation ..................................................... 46 V. Conclusions .............................................................................................................................................. 49 VI. Supplementary material........................................................................................................................... 51 Chapter 2: The genome of the water strider Microvelia longipes provides insights into the role of sexual selection on gene expression and genome architecture. ........................................................................................ 62 I. Abstract ...................................................................................................................................................... 63 II. Introduction .............................................................................................................................................. 64 III. Material and methods .............................................................................................................................. 66 A. Population sampling and culture .......................................................................................................... 66 B. Measurement and statistics ................................................................................................................... 66 C. Sample collection, assembly and annotation of the M. longipes genome ............................................. 66 D. Sample collection and preparation RNA-sequencing ........................................................................... 67 E. Transcriptome assembly, mapping and normalization .........................................................................