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Uhm Phd 9519441 R.Pdf INFORMATION TO USERS This manuscript has been reproduced from the microfilmmaster. UMI films the text directly from the original or copysubmitted. Thus, some thesis and dissertation copies are in typewriter face, while others may be from any type of computer printer. The quality of this reproduction is dependent upon the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleedthrougb, substandard margins, and improper alignment can adversely affect reproduction. In the unlikely. event that the author did not send UMI a complete manuscript and there are missing pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note willindicate the deletion. Oversize materials (e.g., maps, drawings, charts) are reproduced by sectioning the original, beginning at the upper left-hand comer and continuing from left to right in equal sections with smalloverlaps. Each original is also photographed in one exposure and is included in reduced form at the back of the book. Photographs included in the original manuscript have been reproduced xerographically in this copy. Higher quality 6" x 9" black and white photographic prints are available for any photographs or illustrations appearing in this copy for an additional charge. Contact UMI directly to order. UMI A Bell & Howell Information Company 300 North Zeeb Road. Ann Arbor. MI48106-1346 USA 313:761-4700 800:521-0600 Order Number 9519441 Molecular evolution, genetic diversity, and avian malaria in the Hawaiian honeycreepers Feldman, Robert A., Ph.D. University of Hawaii, 1994 D·M-! 300 N.Zeeb Rd. Ann Arbor,MI48106 MOLECULAR EVOLUTION, GENETIC DIVERSITY, AND AVIAN MALARIA IN THE HAWAIIAN HONEYCREEPERS A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAII IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN BIOMEDICAL SCIENCES (GENETICS) DECEMBER 1994 Robert A. Feldman Dissertation Committee: Rebecca L. Cann, Chairperson John A. Hunt Hampton L. Carson Leonard A. Freed Stephen R. Palumbi iii Dedication To my wife Dawn. Her support, guidance, and understanding made this dissertation possible. iv Acknowledgements I gratefully acknowledge the financial and intellectual support of my advisor, Dr. Rebecca Cann. She provided me with the opportunity to work on a fascinating group of organisms in a setting that most graduate students only dream of. She also gave me space to grow, develop and make mistakes. The lessons she taught me I will take far and long remember. I am grateful for the interactions I have had with my "co-advisor" Dr. Leonard Freed. Lenny has not only been a mentor but has become a friend. I will always have fond memories of the times I .spent at Hakalau on those infrequent warm, clear afternoons. I also thank my other committee members, Drs. John Hunt, Hampton Carson and Stephen Palumbi. I have pushed each of you beyond the normal range of graduate student committee member interactions and I thank you for your tolerance. This work was made possible by a number of individuals. The collection of blood samples by Jaan Lepson, Scott Fretz, Eric Vanderwerf, Jobie Rohrer, Bob Peck and Pat Hart was heroic. Excellent laboratory assistance carne from the skilled hands of Leslyn Hanakahi, Beth Laxson and Leila Agullana. George Roderick was patient and giving and I thank him for assistance with the phylogenetic and population data analysis. Carter Atkinson provided blood samples and information used in the malaria study. Yvonne Ching helped v to initiate the malaria project. Jeff Groth provided unpublished cardueline finch sequences used in the phylogenetics chapter. I also thank my lab cohorts, Carol Reeb and Koji Lum for advice, criticism and friendship. I have grown considerably during our time together and I have learned much from both of you. I especially thank you for the space you gave me in the last frantic months when I was attempting to finish and retain some level of sanity. I thank my parents Ed and Ina. You instilled in me a desire to learn, to better myself and provided.me the means to do so. It is through your example that I have come to where I am. Finally, I thank my family, my wife Dawn and our children Daniel and Rachel. The three of you are my treasured blessing and mean more to me than words can say. vi Abstract This dissertation is an interdisciplinary study linking molecular and population genetics to basic problems in island ecology, evolution, and extinction. The Hawaiian honeycreepers (Aves: Fringillidae: Drepanidinae) are extremely morphologically diverse and have radiated into nearly all of the passerine behavioral niches. The group is currently threatened with extinction by anthropogenic disturbances including introduced diseases. Basic biological problems in the honeycreepers include resolving systematic issu~s, documenting population structure and identifying the role of disease in limiting remaining populations. A molecular systematic study tested representative honeycreeper species for monophyly. I sequenced 13 honeycreeper species and used 3 outgroup taxa, 2 cardueline finches and a titmouse, for a 790 bp fragment of the mitochondrial cytochrome b gene. Phylogenetic trees constructed using distance, parsimony, and maximum likelihood methods all grouped the honeycreepers monophyletically and placed P. montana and O. bairdi in a basal clade. Two Ore0mYstis species were polyphyletic, indicating that they have been misclassified. The basis for this misclassification was strong convergence of morphological and behavioral characters associated with insectivory. vii A population study of mitochondrial cytochrome b DNA sequence variability was conducted at three scales; single locations, single islands, and multiple islands. Mitochondrial variation was found for four species living in a center of distribution that is surrounded by highly disturbed regions. In the multiple location study, diversity was found for the Common Arnakihi (Hemignathus virens). The multiple island study showed that a population of Kauai Arnakihi is phylogenetically distinct from those on Maui and Hawaii and that the Maui and Hawaii populations share mitochondrial haplotypes. No variation was detected in the highly mobile Iiwi (Vestiaria coccinea) sampled from the same islands. A PCR-based test for avian malaria was developed that detects the Plasmodium 18S rDNA. Quantitative Competitive PCR experiments established the sensitivity limits of the test. The PCR test was used to estimate prevalence of avian malaria in Hawaiian birds living at high elevations above the normal range of mosquito vectors. Malaria was highest in the nomadic Apapane (Himatione sanguinea) followed by the sedentary Common Arnakihi (Hemignathus virens). Malaria was not detected in the mobile Iiwi (Vestiaria coccinea) . viii Table of Contents Acknowledgements i v Abstract vi List of Tables ..... 0# •••••••••••••••••••••••••••••••••••••••xi List of Figures xii Chapter 1: Background and Introduction 1 The Hawaiian Honeycreepers 3 A Brief History of the Study of Honeycreeper Evolution and Extinction 4 Mitochondrial DNA for Evolutionary Studies and the PCR 8 Questions Addressed in this Dissertation 10 Aspects of Honeycreeper Systematics 10 Hierarchical Aspects of Honeycreeper Mitochondrial DNA Variability 11 Molecular Studies of Avian Malaria in Hawaiian Birds .. 14 Chapter 2: Monophyly of and Polyphyly Within the Hawaiian Honeycreepers 16 Introduction 16 Methods 23 Species Studied 23 Cytochrome b peR and DNA Sequencing 24 Testing for Monophyly 28 Results 33 DNA Sequence Results 33 Discussion 52 Problems with Oreomystis 55 ix General Implications to Honeycreeper Evolution 57 Summary .................................•................ 62 Chapter 3: Intraspecific mtDNA Variability of Hawaiian Honeycreepers 63 Introduction 63 Single Location Study at Hakalau 66 Multiple Locations on the Island of Hawaii 70 Multiple Island Comparison of mtDNA Diversity 71 Methods 73 Sampling of Species and Locations 73 PCR and DNA Sequencing 74 Population Structure Analysis 76 Single Location Comparison 76 Multiple Location Analysis 77 Phylogenetic Analysis of mtDNA Cyt b Sequences 79 Results 81 Single Location Analyses 86 Within Island Comparisons 95 Between Island Comparisons 97 Mitochondrial Population Structure Results 97 Inter-island Phylogenetics of the Amakihi 105 Discussion 109 Summary.•...............................................122 Chapter 4: A peR Test for Avian Malaria in Hawaiian Birds 124 Introduction 124 Methods 128 x Results 139 Proof of PCR Test 139 Sensitivity of PCR Test 142 Surveys of Birds at Upper Elevations 148 Discussion 153 SunlITla-ry. ...•......••••••.•••.••..•••.•.....••.••..•. 160 Chapter 5: Conclusions and Areas for Future Work 161 Further Work on Phylogenetics 161 Further Work on Populations Genetics 163 Further Work on Malaria 164 Literature Cited 166 xi List of Tables Table ~ 2.1 Base Composition by Codon Position 39 2.2 Pairwise Differences 40 3.1 Cyt b Diversity in Honeycreepers 87 3.2 Cyt b Diversity in Birds 120 4.1 Plasmodium Dilution Series 135 4.2 QC-PCR Setup 137 4.3 Smear versus peR 143 4.4 Hakalau, Hawaii Malaria Screening 149 4.5 Hanawi, Maui Malari.a Screening 150 xii List of Figures Figure ~ 2.1 Cyt b DNA Sequence Alignment 34 2.2 Neighbor Joining Distance Tree 42 2 .3 PAUP Tree 43 2.4 Tree 1 vs Tree 2. .· ·· · .··· ·············· . · .45 2.5 Tree 1 vs Tree 3 • ··.···. ················ . ·. .46 2.6 Tree 1 vs Tree 4. .· ·.· ·· · ~ ············
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