DIVERGENCE OF ADAPTIVE PHENOTYPIC TRAITS AND MATE RECOGNITION SYSTEMS (SONG AND COLOR) IN RESPONSE TO RECENT ANTHROPOGENIC HABITAT CHANGES IN AN OCEANIC ISLAND (SÃO TOMÉ, GULF OF GUINEA) ENDEMIC PASSERINE (SPEIROPS LUGUBRIS). Final project report submitted in candidacy for the degree of Biologist ANDREA CAROLINA BAQUERO LOZANO Director: MARTIM PINHEIRO DE MELO PhD. Biology Co-directors: CARLOS DANIEL CADENA PhD. Biology CLAIRE DOUTRELANT PhD. Biology UNIVERSIDAD DE LOS ANDES FACULTAD DE CIENCIAS DEPARTAMENTO DE CIENCIAS BIOLÓGICAS BOGOTÁ D.C., COLOMBIA 2008 ABSTRACT The impact of human activities on natural ecosystems is evident and its consequences are now more profound. The changes in direction and strength of natural and sexual selection that arise in human altered environments due to changes in ecological factors might promote divergence among populations even if these are not isolated, provided selection is sufficiently strong. In birds, such novel selective pressures may lead to divergence in phenotypic traits affecting both ecological adaptation and mate recognition. We examine the effects of recent anthropogenic change in the divergence of some phenotypic patterns of Speirops lugubris, an endemic passerine of Sao Tome Island. Data for morphology, plumage color and song were collected from individuals on both primary forest and shade forest plantations, a habitat less than 200 years-old. Results showed that birds in shade forest plantations were significantly smaller than birds in undisturbed forest however, no plumage color differences between habitats was found. The physical properties of song related to vegetation structure characteristics that differed between habitats and to morphological variation found. This observed change shows that mate recognition signals, a fundamental trait for fitness, are able to respond quickly to habitat changes. This study suggests that the endemic Speirops lugubris is experiencing an adaptive and potentially evolutionary response to diverging habitat structures caused by anthropogenic destruction of the original environment. 1 ACKNOWLEDGMENTS This project has been a great experience both academically and personally. For that I would like to thank Martim Melo, my principal supervisor for this project, who has been supportive and enthusiastic from day one. He suggested and guided this project every step of the way, leading me in the lab and in the field (and getting to the field all the way in São Tomé!). It was a great pleasure working with Martim and learning from him. He was always willing to help and patiently answer questions, even when it took adjusting time schedules for telephone meetings or finding the only computer with working internet in Principe to answer my emails. Martim always was a great motivator and mentor, again I am very grateful. Many thanks go to Claire Doutrelant, who along with Martim Melo, blindly took me in as an intern in the CEFE and gave me the great opportunity of starting this project. She taught and supervised me in all the plumage color analyses and was a great help in the revision of this paper. She was always very welcoming and helped me around the CEFE. I would like to thank Daniel Cadena for willing to co-direct this project, for his great patience, very helpful corrections and guidance. His work and courses have been a big influence in this project and will be a guideline for the future. Special thanks go to Rita Covas was always helpful with suggestions and who along with Martim and Francisca, was a great friend and company in São Tomé, and thereafter. Fieldwork would not have been the same without Rita’s Portuguese lessons, the nice talks and playing around with Francisca. I am grateful to Pablo Stevenson for motivating my interest in ecology and giving me the chance to learn from him in the field several times. I also thank Esteban Payan for helping me with the grant application processes and for his advice. The work in São Tomé was made possible with the help of the Associação Monte Pico, especially my guides Gabriel, Antonio and Señor Pedro. Guillermino, Luis Mario, Lagoas and Georgina were a great help around the island and made me feel at home, as well as Octavio and his family who opened up their home to me. Steffan Andersson and Maria Prager for letting me stay with them when I was ill and kindly providing their house for the last weeks. I am thankful for all the help from people of the Laboratorio de Biología Evolutiva de Vertebrados, Universidad de los Andes in Bogota, Colombia and the Centre d’Ecologie Fontionnelle et Evolutive, CNRS in Montpellier, France. 2 To my friends in the Laboratorio de Biologia Evolutiva de Vertebrados, especially to Angela, Juan Camilo and Carlos P for all their help when writing this paper. Several people helped me along the way. I thank Helena and Manuel, Carmine and Melba, and Jenny Bravo for letting me into their homes on my way to the island. In Montpellier, I would like to thank my dear friends for helping me in several ways. Luisa, Julio, Jenny, Sarah, Douniah, Stephanie, Romain, Laetitia, and Sebastien. I thank Alex Courtiol for his great patience teaching R and helping me with the initial statistics of this project. To my friends in Bogota for being supportive, giving advice and just being there for me. Caya, Camila L, Andres H, Valeria, Lina Q, Lina V, Vicky, Ana G, Ana P, Laura, Alex y Andres P (Mario). Also to Camilo for always helping me out and being there when I needed a little push. Greatest thanks go to my family for always being there for me every step of the way from the very start, even when I was determined to go all the way to São Tomé, which seemed a crazy idea at the time. For understanding and supporting me with my ideas and goals and for bearing with me in times of stress. They endlessly listed to me talk about the project, and motivated me even when they didn’t understand what the excitement was about. Simply for their love and belief in me, thanks. I am very thankful for the financial support for this project, provided by The Rufford Small Grants Foundation for Nature Conservation and The British Ecological Society. 3 TABLE OF CONTENTS Abstract 1 Acknowledgments 2 Contents 4 Introduction 5 Methods 8 Study site 8 Study specie 10 Field sampling 10 Habitat structure measurements 13 Morphological analyses 14 Plumage color analyses 15 Song analyses 16 Results 17 Habitat structure measurements 17 Morphological analyses 18 Plumage color analyses 21 Song analyses 23 Discussion 25 Morphological analyses 25 Plumage color analyses 26 Song analyses 27 Conclusions 28 Future directions 29 References 29 4 INTRODUCTION The impact of human activities on natural ecosystems is ubiquitous. Most research on this fundamental issue has focused on ecological impacts such as describing changes in community composition or in functional disruptions resulting from the loss or gain of particular species (e.g., predators, pathogens, invasive species), and also on following or predicting demographic changes with the goal of preventing species extinctions (Myers et al 2000, Foley et al 2005). Until recently, little attention had been paid to the influences of human action on evolutionary processes, but a growing interest has led to studies evidencing that human-driven evolutionary change is having a widespread impact, posing threats to the natural evolutionary course of species (Seehausen et al 1997, Smith et al 2008, Smith and Bernatchez 2008). Humans can drive phenotypic change in contemporary populations by exposing them to dramatic environmental perturbations that exert novel and strong selective forces driving adaptive divergence over short timescales (Hendry and Kinnison 1999, Reznick and Ghalambor 2001, Palumbi 2001, Stockwell et al 2003, Smith et al 2005, Bell and Collins 2008, Smith et al 2008). Under novel conditions, individuals might survive and reproduce through phenotypic plasticity, and populations might eventually evolve to adapt to such conditions if they harbor sufficient genetic variation to respond to selection (Stockwell et al 2003, Charmantier et al 2008, Hendry et al 2007). Alternatively, environmental perturbations may be too strong for individuals to survive or reproduce successfully, which leads to population declines (Bell and Collins 2008). Accordingly, attention should be directed to understanding and predicting how and under which conditions would populations persist and respond adaptively to the increasingly rapid and strong changes in selective pressures brought about by human activities (Bell and Collins 2008, Hendry et al 2007, Smith and Bernatchez 2008). 5 The changes in direction and strength of natural and sexual selection that arise in human altered environments due to changes in ecological factors might promote divergence among populations even if these are not isolated, provided selection is sufficiently strong (Smith et al 1997, Smith et al 2005, Smith et al 2008). In birds, such novel selective pressures may lead to divergence in phenotypic traits affecting both ecological adaptation and mate recognition (Gibbs and Grant 1987, Badyaev and Leaf 1997, Smith et al 1997, McNaught and Owens 2002, Seddon 2005, Seehausen 2006a). Specifically, morphological characters are often related to variation in feeding ecology, flight performance, and fitness and because these characters are highly heritable in birds (Schluter and Smith 1986, Gibbs & Grant 1987, Smith 1990) they are amenable to diverge even in the face of gene flow (Smith et al 1997). On the other hand, changes in the signaling environment may result in the divergence of traits involved in mate recognition (Endler 1992, Seehausen et al 1997, Boughman 2002) and may eventually lead to the evolution of pre-mating barriers, one of the most important mechanisms in reproductive isolation (Coyne and Orr 2004). Mate recognition systems in birds are commonly based on plumage coloration and acoustic signaling. Plumage color differences among closely related species are often considered to have evolved as a way of minimizing the risk of hybridization; this species isolation hypothesis is supported by cases of reproductive character displacement between taxa in sympatry (McNaught and Owens 2005).