University of North Dakota UND Scholarly Commons Theses and Dissertations Theses, Dissertations, and Senior Projects January 2016 Avian Haemosporidian Parasites From The Brazilian Amazon Jeffrey Andrew Bell Follow this and additional works at: https://commons.und.edu/theses Recommended Citation Bell, Jeffrey Andrew, "Avian Haemosporidian Parasites From The rB azilian Amazon" (2016). Theses and Dissertations. 1873. https://commons.und.edu/theses/1873 This Dissertation is brought to you for free and open access by the Theses, Dissertations, and Senior Projects at UND Scholarly Commons. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of UND Scholarly Commons. For more information, please contact [email protected]. AVIAN HAEMOSPORIDIAN PARASITES FROM THE BRAZILIAN AMAZON by Jeffrey Andrew Bell Bachelor of Science, University of Wisconsin-Green Bay, 1999 Master of Science, North Dakota State University, 2002 A Dissertation Submitted to the Graduate Faculty of the University of North Dakota in partial fulfillment of the requirements for the degree of Doctor of Philosophy Grand Forks, North Dakota May 2016 Copyright 2016 Jeffrey Bell ii This dissertation, submitted by Jeffrey Andrew Bell in partial fulfillment of the requirements for the Degree of Doctor of Philosophy from the University of North Dakota, has been read by the Faculty Advisory Committee under whom the work has been done and is hereby approved. __________________________________________ Dr. Vasyl Tkach, Chairperson __________________________________________ Dr. Jefferson Vaughan __________________________________________ Dr. Rebecca Simmons __________________________________________ Dr. Jason Weckstein __________________________________________ Dr. Catherine Brissette This dissertation is being submitted by the appointed advisory committee as having met all of the requirements of the School of Graduate Studies at the University of North Dakota and is hereby approved. __________________________________________ Wayne Swisher Dean of the School of Graduate Studies __________________________________________ Date iii PERMISSION Title Avian Haemosporidian Parasites from the Brazilian Amazon Department Biology Degree Doctor of Philosophy In presenting this dissertation in partial fulfillment of the requirements for a graduate degree from the University of North Dakota, I agree that the library of this University shall make it freely available for inspection. I further agree that permission for extensive copying for scholarly purposes may be granted by the professor who supervised my dissertation work or, in his absence, by the Chairperson of the department or the dean of the School of Graduate Studies. It is understood that any copying or publication or other use of this dissertation or part thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of North Dakota in any scholarly use which may be made of any material in my dissertation. Jeffrey Andrew Bell April 29th, 2016 iv TABLE OF CONTENTS LIST OF FIGURES ........................................................................................................... ix LIST OF TABLES ............................................................................................................. xi ACKNOWLEDGMENTS ............................................................................................... xiv ABSTRACT .................................................................................................................... xvii CHAPTER I. INTRODUCTION .......................................................................................1 Background on Avian Haemosporidians .........................................1 Life Cycles of Haemoproteus, Plasmodium, and Leucocytozoon ...5 Tools Used for the Detection and Characterization of Avian Haemosporidians............................................................................12 Ecology and Evolution of Host-Parasite Interactions in Avian Haemosporidians............................................................................14 Avian Haemosporidian Studies from South America: Emphasis on the Brazilian Amazon ..............................................19 Study Objectives ............................................................................23 II. MATERIALS AND METHODS ...............................................................25 Study Regions ................................................................................25 Field Collection and Fixation.........................................................26 Laboratory Processing: Light Microscopy .....................................28 Laboratory Processing: Molecular Methods ..................................28 v DNA Extraction .......................................................................29 DNA Amplification Using Real-time and Standard PCR .......29 DNA Sequencing, Sequence Assembly, and Alignment ........35 Evolutionary and Ecological Analysis of Avian Haemosporidians............................................................................37 Phylogenetic Reconstruction ..................................................37 Analysis of Molecular Variance .............................................39 Coevolutionary Analysis ........................................................40 Host Specificity Determination ..............................................43 Composition Analysis ............................................................44 Host Life History Analysis .....................................................45 III. A NEW REAL-TIME PCR PROTOCOL TO DETECT AVIAN HAEMOSPORIDIANS .............................................................................56 Results ............................................................................................56 Discussion ......................................................................................58 IV. AMAZONIAN AREAS OF ENDEMISM DETERMINE THE DISTRIBUTION, DIVERSITY, AND PHYLOGENY OF HAEMOPROTEUS AND PLASMODIUM ................................................62 Results ............................................................................................62 Haemosporidians from Five Brazilian Biomes ......................62 Phylogenetic Reconstruction of Brazilian Haemosporidian Lineages ......................................................69 Haemosporidians from Amazonia ..........................................70 Effect of Amazonian Areas of Endemism on Parasite and Host Communities ...........................................................74 Geographic and Host Taxonomic Structuring of Amazonian Haemosporidian Lineages ...................................74 vi Phylogenetic Reconstruction of Amazonian Haemosporidian Lineages ......................................................76 Phylogeographic Signal within Amazonian Haemosporidian Lineages ......................................................78 Discussion ......................................................................................80 Impact of Amazonia Areas of Endemism on Avian Haemosporidians ....................................................................90 V. HOST LIFE HISTORY CHARACTERISTICS PREDICT INFECTION PROBABILITY OF HAEMOPROTEUS AND PLASMODIUM IN AMAZONIAN BIRDS ..............................................95 Results ............................................................................................95 Impact of Host Life History on Haemosporidian Infection Probability in Amazonia .........................................................96 Impact of Host Life History on Haemosporidian Infection Probability for each Area of Endemism Individually.............98 Discussion ....................................................................................105 VI. COEVOLUTIONARY HISTORY OF AVIAN HAEMOSPOIRIDANS AND THEIR HOSTS FROM GURUPI, BRAZIL ..................................................................................112 Results ..........................................................................................112 Discussion ....................................................................................117 VII. CONCLUSIONS......................................................................................121 Conclusion 1 ................................................................................121 Conclusion 2 ................................................................................122 Conclusion 3 ................................................................................122 Conclusion 4 ................................................................................123 Conclusion 5 ................................................................................123 vii Need for Future Research ............................................................124 APPENDICES .................................................................................................................125 Appendix A. All Haemosporidian Sequences Collected From Brazilian Birds. New Lineages are in Bold and Host Specificity Indices (STD*) are given for all Lineages with More than One Occurrence. .....................................126 Appendix B. Distribution of Avian Haemosporidian Parasites Among all Host Species Collected from Brazil. Haem/Plas Denotes Coinfection with both Haemoproteus and Plasmodium. .........................................................160