Local adaptation by birds to human-altered habitats: the great tit and the house sparrow as model species Sepand Riyahi Aquesta tesi doctoral està subjecta a la llicència Reconeixement 3.0. Espanya de Creative Commons. Esta tesis doctoral está sujeta a la licencia Reconocimiento 3.0. España de Creative Commons. This doctoral thesis is licensed under the Creative Commons Attribution 3.0. Spain License. Local adaptation by birds to human-altered habitats: The great tit and the house sparrow as model species Línea de investigación: Ecología Evolutiva y del Comportamiento Tutoría: Departamento de Biología Evolutiva, Ecología y Ciencias Ambientales – Universidad de Barcelona Centro: Museo de Ciencias Naturales de Barcelona Tesis Doctoral Barcelona, Junio de 2017 Memoria presentada por Sepand Riyahi para optar al grado de Doctor por la Universidad de Barcelona a través del Museo de Ciencias Naturales de Barcelona Juan Carlos Senar Jorda José Domingo Rodríguez Teijeiro Jefe de Investigación Profesor Departamento de Biología Animal Unidad de Ecología Evolutivo Universidad de Barcelona y de la conducta Museo de Ciencias Naturales de Barcelona Cover design: Sahand Riyahi Original photo by Xevi Colome Contents Acknowledgement ......................................................................................................................... 5 List of papers ................................................................................................................................. 6 Report of the director ................................................................................................................... 7 Abstract .......................................................................................................................................... 9 General introduction ................................................................................................................ 10 1. Local adaptation ...................................................................................................................... 10 2. Urbanization ............................................................................................................................ 11 3. Objective ................................................................................................................................. 13 4. Model species: the great tit and the house sparrow ..................................................................... 15 Chapter 1. Evolutionary Genomics of personality traits in the great tit ............................... 16 1.1 Introduction ......................................................................................................................... 16 1.1.1 Natural selection and personality traits in the great tit ............................................................... 16 1.1.2 Measuring the avian personality in the captivity ....................................................................... 17 1.1.3 Candidate genes for personality traits ........................................................................................ 17 1.1.4 DRD4 SNP830 ........................................................................................................................... 18 1.1.5 Epigenetics ................................................................................................................................. 19 1.1.6 Aims ........................................................................................................................................... 20 1.2 Materials and methods ......................................................................................................... 21 1.2.1 Behavioural experiments ............................................................................................................ 21 1.2.2 Gene sequencing ........................................................................................................................ 22 1.2.3 Epigenetic methods .................................................................................................................... 23 1.2.4 Statistical methods ..................................................................................................................... 23 1.3 Results and Discussion ........................................................................................................ 24 1.3.1 DRD4 SNP830 polymorphisms ................................................................................................. 24 1.3.2 Epigenetic effects ....................................................................................................................... 25 Chapter 2. An attempt to identify the genetic basis of the size variation in the black belly melanin stripe of the great tit ..................................................................................................... 29 2.1 Plumage coloration .............................................................................................................. 29 2.2 Candidate gene for black belly melanin stripe in the great tit ............................................. 30 2 2.3 Material and Methods .......................................................................................................... 30 2.4 Results and Discussion ........................................................................................................ 30 Chapter 3. The geographic origin of commensalism in the house sparrow .......................... 31 3.1 Evolutionary history of the house sparrow ......................................................................... 31 3.2 Materials and Methods ........................................................................................................ 32 3.3 Results and Discussion ........................................................................................................ 33 Chapter 4. Natural epigenetic variation within and among six subspecies of house sparrow Passer domesticus ........................................................................................................................ 36 4.1 Epigenetic variation and local adaptation ................................................................................. 36 4.2 Material and Methods ............................................................................................................ 38 4.2.1 Data analyses ............................................................................................................................. 39 4.3 Results and discussion ............................................................................................................ 40 5 General discussion .................................................................................................................. 43 5.1 Isolation by adaptation and urbanization ............................................................................ 43 5.1.1 The role of personality in adaptation to urban habitats .............................................................. 43 5.1.2 Urbanization changes the rules and brakes the personality syndrome ....................................... 45 5.1.3 In search of a genetic link in differences in personality between urban and forest birds ........... 45 5.2 Can epigenetic modifications regulate personality traits? ................................................... 46 5.3 Is MC1R gene polymorphisms responsible for regulating the size of black belly coloration in great tits? ........................................................................................................................................... 47 5.4 Does the house sparrow have a single origin in the Palearctic? .......................................... 48 5.5 Can genome-wide methylation level of house sparrow subspecies explain patterns of adaptation to man-made habitats? ............................................................................................. 48 6 Concluding remarks ................................................................................................................ 49 7 Resumen en Castellano ............................................................................................................ 51 7.1 Introduccion .......................................................................................................................... 51 7.2 Objetivo ................................................................................................................................ 52 7.3 Resultados Y discusión .......................................................................................................... 53 References .................................................................................................................................... 56 PAPER 1 ....................................................................................................................................... 67 Resumen en castellano ................................................................................................................. 67 3 PAPER 2 ....................................................................................................................................... 76 Resumen en castellano ................................................................................................................. 76 PAPER 3 ......................................................................................................................................