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Social Selection, Song Evolution, and the Ecology of Parapatry in Sunbirds

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Social Selection, Song Evolution, and the Ecology of Parapatry in Sunbirds Social Selection, Song Evolution, and the Ecology of Parapatry in Sunbirds by Jay Patrick McEntee A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in Charge: Professor Rauri Bowie, Chair Professor Craig Moritz Professor Frederic Theunissen Spring 2013 1 Abstract Social Selection, Song Evolution, and the Ecology of Parapatry in Sunbirds by Jay Patrick McEntee Doctor of Philosophy in Integrative Biology University of California, Berkeley Professor Rauri Bowie, Chair Social trait evolution can play a critical role in diversification and speciation. In birds, and especially oscine songbirds, the lability, species-specificity, and behavioral functions of song suggest that song divergence may lead or sustain the speciation process. This series of studies focuses on the evolution of song and its consequences in the Eastern Afromontane sky island sunbird species complex, which comprises the Eastern Double-collared Sunbird Nectarinia mediocris and its close relatives. In Chapter 1, I examine the structure of one vocalization type, here termed perched song, for the members of the species complex. I show that song divergence matches molecular phylogenetic reconstructions for six major lineages of the species complex, and that song divergence is multi- dimensional. I use both unsupervised and supervised grouping techniques to assess the distinctness of song phenotypes as measured, with similar results. Model selection after unsupervised clustering analysis suggests that six clusters exist, and these correspond to a priori species distinctions at 92.8%. Model-based discriminant function analysis also correctly identifies songs to the six species designated a priori at 92.8%. The discovery and characterization of the contact zone between Nectarinia moreaui and N. fuelleborni are detailed in Chapter 2. Molecular analyses reveal that there is hybridization, with little or no introgression, between the two species where they meet. The absence of an apparent ecological gradient closely corresponding with the abrupt spatial replacement of one species with the other suggested that interactions between the two species play a strong role in limiting each others’ distribution. To test whether bioclimatic niche divergence is evident between species, I used ecological niche models developed from climate variables associated with species occurrence points. I show that the niches of the two species as characterized are conserved relative to a null distribution as generated by sampling the space within which each species’ distribution is embedded. This test supports the hypothesis that the presence of each species inhibits the expansion of the others’ distribution. Further, I characterize individual genotypes and song and bill length phenotypes sampled in a transect across the contact zone to estimate and compare the width of character clines. Cline analyses show that the genotype and song phenotype clines are roughly coincident and concordant, and very narrow, with the estimated cline width for these two characters ~1.5 km. The bill length cline is offset from the other two clines, and wider. I discuss the many processes that could contribute to the stability and narrowness of the genotype and song clines, including conspecific clumping. 2 In Chapter 3, I present the results of two playback experiments performed to examine male territorial responses to divergent signals in the parapatrically distributed N. moreaui and N. fuelleborni. These two species have diverged greatly in song phenotype, and subtly in morphometric and plumage traits. The first of the two experiments examines responses to multimodal signaling by assessing reactions to mount/song playback combinations, which are crossed for the two species. This experiment resulted in asymmetric heterospecific response between the two species, with N. moreaui responding consistent with predictions based on the species recognition hypothesis, and N. fuelleborni failing to respond more frequently to its own song than to N. moreaui song. Duration of response by treatment did not correspond to expectations based on species recognition, as there was a trend for individuals to respond longer to heterospecific mounts. In the second experiment, I investigated geographic variation in territorial response to the sibling species compared to own species’ song and an ecologically relevant control stimulus, in the form of the song of a sunbird that co-occurs with both species for all tested populations. Responses to the control species were infrequent. Geographic variation in response differences to heterospecific (sibling taxon) and conspecific songs occurs. Strong responses to heterospecifics were not limited to the area of contact in N. fuelleborni, suggesting a role for stochastic processes in the evolutionary loss of response to the sibling taxon’s song. To conclude, song divergence accompanies molecular divergence in the Eastern Afromontane sky island sunbird species complex. Its role in the speciation process might be quite complex, and not as simple as the correlated evolution of female preference with male phenotype as in a Fisherian runaway process. I suggest that one role of song divergence during allopatric or parapatric speciation may be to reduce co-occurrence of individuals with dissimilar song phenotypes through anisotropic dispersal. i To the people of eastern Africa, and especially the Tanzanian wananchi, for all they’ve taught me. Shukrani. To the late Theodore A. Parker III, for inspiration. To my dad, who put names to different kinds of birds when I was young. And to Kathleen Rudolph, who corralled my head whenever it started to get away. ii Table of contents Chapter 1 1 Chapter 2 24 Chapter 3 61 Literature cited 88 Appendix 100 iii Acknowledgements Permission for field research in Tanzania was furnished at the national level by the Tanzania Wildlife Research Institute (TAWIRI) and the Commission for Science and Technology (COSTECH), Tanzania. Further national permissions for use of public lands in Tanzania were granted by the Ministry of Natural Resources, Forestry and Beekeeping Division. Permissions for field research in Kenya were granted through the National Museum of Kenya and the National Council for Science and Technology. In particular I thank Muchane Muchai of the National Museum of Kenya for supporting these research efforts. The Kenya Wildlife Service furnished permissions to work in Aberdares National Park. Permission for field research in Mozambique was granted through the Universidade Eduardo Mondlane Natural History Museum of Maputo and the Ministry of Agriculture. Museum access was provided by Kimball Garrett (Los Angeles County Museum), Jon Fjeldså, and the staff of the Museum of Vertebrate Zoology. Sandra Perello assisted with museum research. Sound cataloguing assistance was performed by Nadje Najar, Emilia Wakamatsu, Addien Wray, Jessica Hughes, Somin Lim, Violet Kimzey, and Kyle Marsh. Maneno Mbilinyi, Elia Mulungu, Chacha Werema, Sylvester Karimi, and Dalila Sequeira contributed exceptional research assistance in the field. Many others contributed research assistance for short periods of time, and their work is greatly appreciated. Justyn Stahl provided crucial moral support for field work. A number of people hosted me during my field excursions, including David Taylor and Jenny Woodier, Sarah McGregor, Dalila Sequeira and family, and Shanna Sheridan-Johnson and family. Chacha Werema, David Moyer, Norbert Cordeiro, Liz Baker and Neil Baker gave invaluable support and advice for field research. Anna Sellas and Lydia Smith contributed expertise in the molecular laboratory. Joshua Penalba performed much of the laboratory component of the molecular work. Josh was particularly invaluable to the success of this entire effort. A number of lab and discussion groups provided especially important feedback on research, namely the Rauri Bowie lab group and the Animal Behavior Lunch Seminar group at UC Berkeley and the Rebecca Kimball/Ed Braun and Scott Robinson lab groups at the University of Florida. The ‘Endler reading group’ at UC Berkeley was a constant source of new ideas. Jon Fjeldså provided critical background information and natural history knowledge regarding Eastern Afromontane birds. Funding for this research was generously provided by the Museum of Vertebrate Zoology, the UC Berkeley Department of Integrative Biology, a UC Berkeley Center for African Studies Rocca Scholarship, a National Science Foundation Doctoral Dissertation Improvement Grant, a National Science Foundation Graduate Research Fellowship, a National Geographic Society/Waitt Foundation Grant, the American Ornithologists’ Union, the Explorers Club, and the Mohamed bin Zayed Species Conservation Fund. Kathleen Rudolph assisted with virtually every aspect of this work. iv My committee members provided valuable insight, feedback, and recommendations. Their suggestions were often prescient. Craig Moritz was particularly helpful with regard to the development of the contact zone work. Frederic Theunissen advised me regarding bioacoustics analyses. Rauri Bowie, my committee chair and adviser, was always interested and enthusiastic in discussing field plans and new results, and provided extensive direction regarding the collection and analysis of molecular data. 1 CHAPTER 1 Song structure and divergence in the Eastern Afromontane sky island sunbird
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