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Evolution of Social Structure of the Ant Genus Myrmecia Fabricus (Hymenoptera: Formicidae

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Evolution of Social Structure of the Ant Genus Myrmecia Fabricus (Hymenoptera: Formicidae ResearchOnline@JCU This file is part of the following reference: Qian, Zengqiang (2012) Evolution of social structure of the ant genus Myrmecia fabricus (Hymenoptera: Formicidae. PhD thesis, James Cook University. Access to this file is available from: http://eprints.jcu.edu.au/25180 The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please contact [email protected] and quote http://eprints.jcu.edu.au/25180 Evolution of Social Structure in the Ant Genus Myrmecia Fabricius (Hymenoptera: Formicidae) Thesis submitted by Zengqiang QIAN MSc in January 2012 For the degree of Doctor of Philosophy in Tropical Ecology and Zoology within the School of Marine and Tropical Biology James Cook University Townsville, Queensland, Australia TABLE OF CONTENTS LIST OF FIGURES………...…………………………………………………………i LIST OF TABLES……………………………………………………………………ii ACKNOWLEDGEMENTS………………………………………………………iii CONTRIBUTIONS OF OTHERS….………………………………………………iv PUBLICATIONS ARISING FROM THIS THESIS……………………………v ABSTRACT………………………...………………………………………………vi CHAPTER 1: General Introduction………...………………………………………1 Background…………………..……………………………………………………1 Colony structure of eusocial insects……………………………………………………1 The Australian bulldog or jumper ant genus Myrmecia Fabricius…..……………3 Objectives and outline of the thesis………………………………………………4 CHAPTER 2: Polymorphic EST-Derived Microsatellites in the Fire Ant Solenopsis invicta and Their Cross-Taxa Transferability in the Bulldog Ant Myrmecia brevinoda and the Black Tree Ant Tetraponera punctulata……………6 Abstract……………………………………………………………………………6 Introduction……………………..…………………………………………………7 Materials and methods…………….………………………………………………9 Primer design……………..………………………………………………………………9 PCR amplification and genotyping analysis….………………………………………9 Data analysis……………………….……………………………………………………10 Results and discussion……………………………………………………………10 CHAPTER 3: Characterization of Polymorphic Microsatellites in the Giant Bulldog Ant Myrmecia brevinoda and the Jumper Ant M. pilosula……………12 Abstract………………….………………………………………………………12 Introduction………………………………………………………………………13 Materials and methods………...…………………………………………………14 Insect samples and DNA extraction……..……………………………………………14 Microsatellite isolation…………………………………………………………………15 PCR amplification and genotyping analysis…………..……………………………16 Data analysis………………………….…………………………………………………16 Results………………………….………………………………………………19 Discussion…………………………………………………………………………20 CHAPTER 4: Intraspecific Support for the Polygyny-vs.-Polyandry Hypothesis in the Bulldog Ant Myrmecia brevinoda…………………………………………21 Abstract…………………………………………………………………………21 Introduction………………………………………………………………………22 Materials and methods…………...………………………………………………25 Insect samples and DNA extraction…………..………………………………………25 Microsatellite genotyping………………………………………………………………25 Statistical analyses……………….……………………………………………………26 Results……………………………………………………………………………29 Basic population genetics and identification of colony boundaries….….….……29 Queen mating frequency and paternity skew……….…………….…………………31 Intracolonial relatedness………….…….…….….……………………………………31 Number of queens and maternity skew……………….………………………………33 Polygyny vs. polyandry…………………………………………………………………33 Discussion…………………………………………………………………………33 Queen number, mating frequency and dispersal……………………………………33 Polygyny vs. polyandry…………………………………………………………………36 CHAPTER 5: Nestmate Recognition in the Facultatively Polygynous Bulldog Ant Myrmecia brevinoda…………………………………………………………………39 Abstract…………………………………………………………………………39 Introduction………………………………………………………………………40 Materials and methods…………………………………………………………42 Ant sampling……………….….…………………………………………………………42 Behavioural assays……………..………………………………………………………43 Statistical analyses………………….…….….…………………………………………44 Results…………………….………………………………………………………45 Discussion…………………………………………………………………………49 CHAPTER 6: Colony Genetic Structure in the Australian Jumper Ant Myrmecia pilosula…………………………….…………………………………………………52 Abstract…………………….……………………………………………………52 Introduction………………………………………………………………………53 Materials and methods…………………………………………………………55 Field sampling, DNA extraction and microsatellite genotyping…………………55 Marker evaluation and population genetic estimates………………………………57 Estimation of relatedness………………………………………………………………58 Queen numbers, queen-mating frequencies and reproductive skew…….….….…58 Results………………………….………….………………………………………59 Basic population genetics and identification of colony boundaries….…….….…59 Queen mating frequency and paternity skew……….……….………………………61 Intracolonial relatedness………………………………………………………………61 Number of queens and maternity skew……….………………………………………63 Polygyny vs. polyandry…………………………………………………………………63 Discussion…………………………………………………………………………63 Queen-mating frequency and dispersal………………………………………………63 Polygyny vs. polyandry…………………………………………………………………66 CHAPTER 7: General Discussion…………………………………………………68 Summary of key findings……….…….…………………………………………68 Polygyny vs. polyandry…………………………………………………………………68 Queen dispersal and colony foundation….…….……………………………………69 Nestmate recognition…….………….….………………………………………………69 Future directions…………………………………………………………………70 REFERENCES……………………………………………………………………73 APPENDICES………………………………………………………………………94 Appendix I: AI-based internest aggression matrix in M. brevinoda…….……94 Appendix II: MAI-based internest aggression matrix in M. brevinoda………95 Appendix III: MAS-based internest aggression matrix in M. brevinoda….…96 LIST OF FIGURES Chapter 4 Fig. 4.1 Schematic map of Myrmecia brevinoda colonies…………..………………25 Fig. 4.2 Correlation between geographic and genetic distances for pairs of Myrmecia brevinoda nests (r = 0.013, P = 0.420; 9999 permutations) ….….…………28 Fig. 4.3 Estimated (a) and pedigree-effective (b) number of matings per queen in Myrmecia brevinoda…………………………….………….………………30 Fig. 4.4 The relationship across colonies of Myrmecia brevinoda between polygyny, measured as the number of queens per colony, and polyandry, measured as the mean estimated (a) or pedigree-effective (b) number of matings per queen……………………….………….……………………………………32 Chapter 5 Fig. 5.1 Schematic map of Myrmecia brevinoda colonies…….………….….………42 Fig. 5.2 Mantel’s correlations among internest distance and aggression matrices…46 Fig. 5.3 Observed within- (a) and between-nest (b) aggression levels in Myrmecia brevinoda……………………………………………………………………47 Chapter 6 Fig. 6.1 Schematic map of Myrmecia pilosula colonies……….……….……………55 Fig. 6.2 Correlation between geographic and FST genetic distances for pairs of Myrmecia pilosula nests (r = 0.324, P = 0.046; 9999 permutations)………60 Fig. 6.3 Correlation between geographic and FST genetic distances for pairs of Myrmecia pilosula nests (r = 0.403, P = 0.040, 9999 permutations)………60 Fig. 6.4 Estimated (a) and pedigree-effective (b) number of matings per queen in Myrmecia pilosula….……….………….………….………….……………62 i LIST OF TABLES Chapter 2 Table 2.1 Characterization of 12 polymorphic EST-derived microsatellite loci in Solenopsis invicta (n = 24).……..…………….….………………………8 Table 2.2 Cross-taxa amplification of EST-derived microsatellite loci in distantly -related species………….……………………….………………………11 Chapter 3 Table 3.1 Characterization of polymorphic microsatellite loci in M. brevinoda and M. pilosula, and amplifiability in M. pyriformis……………………………17 Table 3.2 Transferability and utility of candidate microsatellite loci in M. brevinoda and M. pilosula…………………..………………………………………19 Chapter 4 Table 4.1 Characteristics of the colonies used to study colony genetic structure in Myrmecia brevinoda…………….….……………………………………24 Table 4.2 Relatedness among workers in the colonies of Myrmecia brevinoda…..…29 Chapter 5 Table 5.1 Aggression scale used to score interactions among workers of Myrmecia brevinoda……………………..……….…………………………………43 Table 5.2 Mantel’s correlations among internest distance and aggression matrices…45 Table 5.3 Pairwise comparisons of internest aggression levels among various social form combinations using two-tailed independent-samples t-tests….……48 Table 5.4 Pairwise comparisons of internest aggression levels among nests with different levels of worker-worker relatedness using two-tailed independent-samples t-tests……………………………………………48 Chapter 6 Table 6.1 Characteristics of the colonies used to study colony genetic structure in Myrmecia pilosula………………….……………………………………56 ii ACKNOWLEDGEMENTS Many people and organizations have provided valuable assistance during my PhD candidature. In particular, I wish to express my sincere gratitude to: My supervisors Prof. Ross H. Crozier, A/Prof. Simon K. A. Robson, Dr. Helge Schlüns, Prof. Birgit C. Schlick-Steiner and Dr. Florian M. Steiner for their continuous guidance, advice and encouragement. Without their patient supervision, the completion of this thesis would have been impossible. Ching Crozier for her assistance in sample collection and her technical guidance in the laboratory. Your rich knowledge of molecular biology has left me a deep impression. All other members of the Crozier lab over the years, especially Ellen Schlüns, Faye Christidis, Itzel Zamora-Vilchis, F. Sara Ceccarelli, Philip S. Newey and Melissa E. Carew, for their valuable help and friendly advice. Working with you has been a pleasant and inspiring experience. The Department of Education, Employment and Workplace Relations (Australia) for financial support to cover tuition fees and living expenses during my PhD candidature. The School of Tropical Biology at James Cook University
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