Extreme Worker Polymorphism in the Big-headed Pheidole Ants Item Type text; Electronic Dissertation Authors Huang, Ming Hua Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 03/10/2021 05:41:47 Link to Item http://hdl.handle.net/10150/247257 1 EXTREME WORKER POLYMORPHISM IN THE BIG-HEADED PHEIDOLE ANTS by Ming Hua Huang ________________________________ A Dissertation Submitted to the Faculty of the DEPARTMENT OF ENTOMOLOGY In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2012 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Ming Hua Huang entitled Extreme worker polymorphism in the big-headed Pheidole ants and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy _________________________________________________________ Date: 09/19/2012 Diana Wheeler _________________________________________________________ Date: 09/19/2012 Wulfila Gronenberg _________________________________________________________ Date: 09/19/2012 Anna Dornhaus _________________________________________________________ Date: 09/19/2012 Daniel Papaj Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College. I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. _________________________________________________________ Date: 09/19/2012 Dissertation Director: Diana Wheeler 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library. Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the author. SIGNED: Ming Hua Huang 4 ACKNOWLEDGMENTS I am eternally grateful to my academic advisor Diana Wheeler for introducing me to Pheidole ants and trusting in my ability to perform the research required to decipher the mysteries of this charismatic and enigmatic study system. She has shown an uncanny ability to nurture me throughout my graduate career without ever stifling my need to explore openly and work independently. Retrospectively, these are all genuine characteristics of an academic mother, in the truest sense. Her depth of knowledge and her incredible office library collection are quite impressive, both of which are sources I have relied on in many occasions during my PhD. Many thanks also to my committee members (Wulfila Gronenberg, Anna Dornhaus, and Dan Papaj) for being patient and offering me guidance whenever it was needed. I thank Norm Buck, Toby Daly-Engel, Kirk Anderson, Pedro Rodrigues, Michele Lanan, and Lesley Washburn from the Wheeler lab for their endless words of encouragement and open exchange of research ideas. I am especially grateful for everything that I have learned from Norm Buck, which ranged from general ant husbandry to sophisticated molecular biology techniques. He has always been more than willing to share his ever-spewing wealth of knowledge if one was patient enough to listen. Special thanks also goes to Toby Daly-Engel and Kirk Anderson for taking time to mentor me on my microsatellite studies even after they had moved on to faculty and research scientist positions elsewhere. My graduate studies have been such a rich experience due to the help and support of a large community of incredible staff and research scientists within and outside of the Entomology department in the University of Arizona (UA). Everyone in the Dornhaus, Gronenberg, and Hunter labs have provided me with invaluable resources. I specifically thank Yves Carrière and Jenny Jandt for statistical advice. Thanks also to all the researchers and staff at the USDA Carl Hayden Honey Bee Laboratory, especially Gloria Degrandi-Hoffman, Bruce Eckholm, Brendon Mott, Tim Sheehan, and Vanessa Corby-Harris. I thank my researcher collaborators outside of UA, including Ehab Abouheif (McGill University, Canada), Else Fjerdingstad (formerly Queens College, NY), and Jürgen Gadau (Arizona State University), for playing critical roles in broadening my areas of expertise. I am extremely grateful for the support and field assistance of many close friends here in AZ, especially Aaron Chambers, Alex Yelich, Jennifer Patton, Aaron Beyerlein, Joe Deas, and Tuan Cao. I am truly thankful for the ongoing support and understanding of my parents, Bi Xing and Yin You Huang, even though a pursuit of a career in entomology is not exactly something they are accustomed to. I also really appreciate the efforts of my brother, Ming Hui Huang, for putting my mind at ease by taking great care of my parents as I pursue my career from afar. My graduate experience has been funded by the USDA Carl Hayden Bee Lab, Center for Insect Science (CIS), and BioME and CATTS GK-12 programs. Relevant travels to conferences have been funded by awards from the H.E. Carter Foundation, GPSC, CIS, IUSSI society, and Under-represented Graduate Student program. 5 TABLE OF CONTENTS ABSTRACT…………………………………………………………………………………………………………..6 INTRODUCTION………………………………………………………………………………………………......8 PRESENT STUDY………………………………………………………………………………………………..14 REFERENCES……………………………………………………………………………………………………..18 APPENDIX A. COLONY DEMOGRAPHICS OF RARE SOLDIER-POLYMORPHIC WORKER CASTE SYSTEMS IN PHEIDOLE ANTS (HYMENOPTERA: FROMICIDAE) ...……………...…………..……………………...…………………………………...21 APPENDIX B. FOOD PROCESSING ROLES AND ADAPTIVE MORPHOLOGY OF DIFFERENT WORKER CASTES IN SOLDIER-POLYMORPHIC PHEIDOLE ANTS ……………………………………………………………………………………………………...58 APPENDIX C. MULTI-PHASE DEFENSE BY THE BIG-HEADED ANT PHEIDOLE OBTUSOSPINOSA AGAINST RAIDING ARMY ANTS ………………….………………...89 APPENDIX D. MATING SYSTEM EVOLUTION AND WORKER CASTE DIVERSITY IN PHEIDOLE ANTS .………………………………………………….…………..110 APPENDIX F. PERMISSIONS ……………………………………………………………………………..152 6 ABSTRACT Polymorphism is the existence of multiple phenotypes within a given species in a population. In social insects, worker polymorphism plays a key role in maximizing the effectiveness of the division of labor. Some ants have an extreme form of worker polymorphism where workers have a broad size range and multiple size modes. Pheidole ants, for example, consist of both highly polymorphic species as well as those with relatively low polymorphism. Here, we examined why different Pheidole species have different degrees of polymorphism and how polymorphism is produced. We thoroughly characterized the worker caste systems of P. spadonia, P. rhea, P. obtusospinosa, and P. tepicana. There were significant differences among the four species in size range, number of size modes, caste ratios, allometry, and caste biomass allocation. An examination of worker caste traits of P. spadonia, P. rhea, and P. obtusospinosa revealed that as head size increased for all three species: (1) mandibles became broader and less serrated, (2) head muscle volume increased, and (3) bite force increased. These traits of large supersoldiers are likely adapted for crushing while those of small minors are likely for cutting. Foraging experiments showed that P. spadonia, P. rhea, and P. obtusospinosa used their workforce in different ways for food processing outside the nest. For P. rhea, the frequency of supersoldiers involved in food processing increased as the processing level required increased. However, P. obtusospinosa supersoldiers were rarely found processing food outside the nest and P. spadonia soldiers assisted in processing dead prey but did not help at all in processing live prey. P. obtusospinosa and P. spadonia workers 7 may be more involved with other colony tasks. This hypothesis was confirmed when field observations of P. obtusospinosa showed supersoldiers participating in head- blocking at their entrance to fend off invading army ants; no other castes exhibited this behavior. Lastly, we tested genetic influences on worker polymorphism. We found that as colony genetic diversity increased (via polyandry), the degree of polymorphism increased. We also showed evidence of paternal genes influences on the development of worker castes in the highly polymorphic P. rhea. 8 INTRODUCTION An explanation of the problem and review of literature Polymorphism is defined as the expression of multiple phenotypes within the same species in a population as a result of differences in exposure to environmental stimuli or genotype (West-Eberhard 2003). Examining this phenomenon is important because it is very common in the animal kingdom and it often helps reveal the contrasting selective pressures acting on groups of organisms that occupy different ecological niches. In solitary organisms, polymorphisms help increase the fitness of individuals in a population in response to changing environments or adoption of different