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INSIGHTS FROM AVIAN DIVERSIFICATION PATTERNS IN THE GUINEO- CONGOLIAN TROPICAL LOWLAND FORESTS A Dissertation by JERRY WALLACE HUNTLEY Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Gary Voelker Committee Members, Jessica Light Kevin Conway Gregory Sword Head of Department, Michael Masser August 2017 Major Subject: Wildlife and Fisheries Sciences Copyright 2017 Jerry Huntley ABSTRACT The biogeographical history of the Afro-tropical Guineo-Congolian lowland forests during the Plio-Pleistocene is characterized by pervasive fragmentation- coalescence cycling due to global climatic oscillations. Vicariance scenarios driven by forest fragmentation have long been hypothesized as major mechanisms for the creation and maintenance of Afro-tropical avian diversity. However, the timing and center of diversification events remains unclear. Additionally, the current paradigm within the field regards the Guineo-Congolian forests as regions of little importance in creating genetic diversity patterns. The goal of this dissertation is to address, using multiple levels of evidence, potential avian diversification patterns across Sub-Saharan lowland tropical forests. Utilizing molecular data from 75 avian species, we undertook a combination of molecular and biogeographic methods to construct time-calibrated phylogenies, ancestral area estimations, haplotype networks, and diversification rate estimations. We found substantial, geographically discrete genetic structuring in the majority of sampled avian species, much of it dating to the Pleistocene epoch. Additionally, ancestral area estimations reconstruct the lowland forests as the area of origin the ancestor of our two highest sampled genera. Diversification rates estimated for three genera recovered increasing diversification rates throughout the Plio-Pleistocene. Our results strongly indicate that lowland tropical forests are potentially harboring much more cryptic avian genetic diversity than previously hypothesized. The prevailing view ii of the Guineo-Congolian forests as regions that have been responsible for the creation of genetic diversity does not appear to be appropriate for many of the avian species sampled here. Specifically, understory taxa, which are heavily tied to the dark, dense parts of the lowland tropical forests showed the most substantial levels of genetic distance between geographic regions. These results highlight the importance of considering behavioral ecology when studying the biogeographic history of forest taxa. Overall, the data from this study signals that climate-induced forest fragmentation in the Plio-Pleistocene undoubtedly played a substantial role in the cyclical creation of new avian diversity in the Guineo-Congolian forests of Africa. iii DEDICATION This dissertation is dedicated to my family: Scott, Terrie, Laurie, Kevin, Kristin, and Harper Huntley. iv ACKNOWLEDGEMENTS I would like to thank my committee chair, Dr. Gary Voelker, for all the years of patience, guidance, and support. Additionally, I thank all of my committee members for their timely guidance and advice through the entire process. I wish to acknowledge Dr. Jessica Light for all the advice and Dr. Ben Marks for early and formative conversations about the birds of Africa. I would like to thank Drs. Toby Hibbitts and Graeme Oatley for large contributions to field work in Benin and South Africa, respectively. Thank you to my many lab mates over the years (including members of the Light lab) for keeping the lab atmosphere fun and constructive. I would like to acknowledge the curators, collections managers, and all others contributing to the natural history collections from which many of my tissue samples were obtained. The importance of natural history collections to the investigation of biodiversity cannot be overstated. In specific, I would like to thank all of the personnel at the Biodiversity, Research, and Teaching Collections of Texas A&M University for all that I’ve learned from them over the years. Thank you to all the friends that have made my time at Texas A&M University special. Specifically, thank you Johanna Harvey for over a decade of support and friendship. And finally, thank you to my family for all of your support and patience. v CONTRIBUTORS AND FUNDING SOURCES Contributors This dissertation was supervised by a doctoral committee consisting of Dr. Gary Voelker (advisor) and Dr. Jessica Light of the Department of Wildlife and Fisheries Sciences, Dr. Kevin Conway of the Department of Wildlife and Fisheries Sciences, and Dr. Gregory Sword of the Department of Entomology. The BEAST analyses in Chapters II, III, and IV were made possible with the assistance of Johanna Harvey of the Department of Wildlife and Fisheries Sciences. Chapter IV was edited by Dr. Marco Pavia of the University of Torino and Dr. Giovanni Boano of the Museo Civico di Storia Naturale in Carmagnola, Italy. All other work conducted for the dissertation was completed by the student independently. Funding Sources This work was made possible in part by the Frank M. Chapman Memorial Fund from the American Museum of Natural History. Graduate study was supported by the Willie Mae Harris Graduate Fellowship from the College Of Agriculture and Life Sciences at Texas A&M University. vi NOMENCLATURE ACO1 Aconitase 1 intron-10 ATP6 ATPase subunit 6 BAMM Bayesian analysis of macroevolutionary mixtures BEAST Bayesian analysis of macroevolutionary mixtures Bp Base pairs C Congo forest block CAR Central African Republic COI Cytochrome oxidase I CYTB Cytochrome oxidase beta DEC Dispersal-extinction cladogenesis DEC+J Dispersal-extinction cladogenesis plus jump dispersal DNA Deoxyribonucleic acid DRC Democratic Republic of the Congo EG Equatorial Guinea EGG Equatorial Guinea/Gabon GTR General time reversible Ka Thousand years ago LG Lower Guinean forest block LRT Likelihood ratio test Ma Million years ago vii MCMC Markov chain Monte Carlo MSH Montane Speciation Hypothesis mtDNA Mitochondrial deoxyribonucleic acid MYO Myoglobin intron 2 N Number ND2 NADH-dehydrogenase subunit 2 nuDNA nuclear deoxyribonucleic acid p Pairwise PCR Polymerase chain reaction PFRH Pleistocene Forest Refuge Hypothesis PP Posterior probability RBH Riverine Barrier Hypothesis RSA Republic of South Africa SD Standard deviation SLL Sierra Leone/Liberia TGF β2 Transforming growth factor beta 2 UG Upper Guinean forest block viii TABLE OF CONTENTS Page ABSTRACT .......................................................................................................................ii DEDICATION .................................................................................................................. iv ACKNOWLEDGEMENTS ............................................................................................... v CONTRIBUTORS AND FUNDING SOURCES ............................................................. vi NOMENCLATURE .........................................................................................................vii TABLE OF CONTENTS .................................................................................................. ix LIST OF FIGURES ........................................................................................................... xi LIST OF TABLES ......................................................................................................... xiii CHAPTER I INTRODUCTION ....................................................................................... 1 CHAPTER II A TALE OF THE NEARLY TAIL-LESS: THE SYSTEMATICS AND BIOGEOGRAPHY OF THE AVIAN GENUS SYLVIETTA (CROMBECS) ................... 4 II.1 Introduction ............................................................................................................. 4 II.2 Methods ................................................................................................................. 10 II.3 Results ................................................................................................................... 15 II.4 Discussion .............................................................................................................. 22 CHAPTER III CRYPTIC DIVERSITY IN AFRO-TROPICAL LOWLAND FORESTS: THE SYSTEMATICS AND BIOGEOGRAPHY OF THE AVIAN GENUS BLEDA (BRISTLE-BILLS) ............................................................................... 31 III.1 Introduction .......................................................................................................... 31 III.2 Methods ................................................................................................................ 37 III.3 Results .................................................................................................................. 41 III.4 Discussion ............................................................................................................ 54 CHAPTER IV THE IMPACT OF PLIO-PLEISTOCENE FOREST FRAGMENTATION ON AFRO-TROPICAL AVIAN DIVERSITY: THE SYSTEMATICS AND BIOGEOGRAPHY OF THE GENUS CRINIGER (BEARDED GREENBULS) ............................................................................................ 63 ix IV.1 Introduction .......................................................................................................... 63 IV.2 Methods ................................................................................................................ 71 IV.3 Results