Evolution of social structure in the ant genus Myrmecia fabricius (Hymenoptera: Formicidae)
13
0
0
Full text
(2) 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.
(3) 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.
(4) 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.
(5) 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.
(6) 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.
(7) 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.
(8) 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.
(9) 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 and the Australian Research Council (ARC) for financial support to cover costs associated with the research. Hui Cao and Yuxin Fu for their assistance in field survey and sample collection. Dr. Robert W. Taylor for his assistance in sample collection and identification. Ainsley Calladine for his assistance in microsatellite genotyping. Staff at the School of Marine and Tropical Biology (JCU) for their general daily support. Two examiners for their critical comments and constructive suggestions on the earlier version of this thesis. My wonderful family for their unconditional love and understanding during these years. iii.
(10) CONTRIBUTIONS OF OTHERS. People and organizations, who have substantially contributed to the major chapters of this thesis, have been acknowledged in details in the following table. Chapters. 2. 3. 4. 5. 6. Idea. ZQ. ZQ, RC. ZQ, RC. ZQ, RC. Study design. ZQ. ZQ, FC, MC, RC ZQ, FC, MC. ZQ, RC. ZQ, RC. Sample collection. ZQ, RC, CC. ZQ, RC, CC. ZQ, YF. ZQ, RC, BS, FS ZQ, YF. Data collection. ZQ, CC. ZQ, FC, MC. ZQ. ZQ. ZQ. Data analyses. ZQ, RC. ZQ. ZQ, SR. ZQ, SR. ZQ. Manuscript preparation. ZQ, RC, BS, FS. ZQ, FC, MC, BS, FS, HS. ZQ, BS, ES, FS, HS, SR. ZQ, BS, ES, FS, HS, SR. ZQ, BS, ES, FS, HS, SR. Financial support. ARC, DEEWR, SMTB. ARC, DEEWR, SMTB. ARC, DEEWR, SMTB. ARC, DEEWR, SMTB. ARC, DEEWR, SMTB. RC, CC. BS = Birgit C. Schlick-Steiner; CC = Ching Crozier; ES = Ellen A. Schlüns; FC = F. Sara Ceccarelli; FS = Florian M. Steiner; HS = Helge Schlüns; MC = Melissa E. Carew; RC = Ross H. Crozier; SR = Simon K. A. Robson; YF = Yuxin Fu; ZQ = Zengqiang Qian ARC = Australian Research Council; DEEWR = the Department of Education, Employment and Workplace Relations, Australia; SMTB = School of Marine and Tropical Biology, James Cook University. Supervised by: Prof. Ross H. Crozier, James Cook University (Australia) Assoc./Prof. Simon K. A. Robson, James Cook University (Australia) Dr. Helge Schlüns, James Cook University (Australia) Prof. Birgit C. Schlick-Steiner, University of Innsbruck (Austria) Dr. Florian M. Steiner, University of Innsbruck (Austria) iv.
(11) PUBLICATIONS ARISING FROM THIS THESIS. Peer-reviewed journal articles: Qian Z-Q, Crozier YC, Schlick-Steiner BC, Steiner FM, Crozier RH (2009) Characterization of expressed sequence tag (EST)-derived microsatellite loci in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Conservation Genetics, 10, 1373-1376. Qian Z-Q, Ceccarelli FS, Carew ME, Schlüns H, Schlick-Steiner BC, Steiner FM (2011) Characterization of polymorphic microsatellites in the giant bulldog ant, Myrmecia brevinoda and the jumper ant, M. pilosula. Journal of Insect Science, 11, 71. Qian Z-Q, Schlüns H, Schlick-Steiner BC, Steiner FM, Robson SKA, Schlüns EA, Crozier RH (2011) Intraspecific support for the polygyny-vs.-polyandry hypothesis in the bulldog ant Myrmecia brevinoda. Molecular Ecology, 20, 3681-3691. Qian Z-Q, Robson SKA, Steiner FM, Schlick-Steiner BC, Schlüns EA, Schlüns H, Crozier RH (2011) Intraspecific aggression in the facultatively polygynous bulldog ant Myrmecia brevinoda, 20, 3681-3691. Qian Z-Q, Schlick-Steiner BC, Steiner FM, Robson SKA, Schlüns H, Schlüns EA, Crozier RH (2012) Colony genetic structure in the Australian jumper ant Myrmecia pilosula. Insectes Sociaux, 59, 109-117. Conference abstract: Qian Z-Q, Robson SKA, Schlüns H, Schlüns EA, Schlick-Steiner BC, Steiner FM, Crozier RH (2010) Colony structure in three species of the ant genus Myrmecia. XVI Congress of the International Union for the Study of Social Insects, Copenhagen, Denmark.. v.
(12) ABSTRACT. Eusocial insects vary significantly in colony queen number and mating frequency, resulting in a wide range of social structures. Detailed studies of colony genetic structure are essential to elucidate how various factors affect the relatedness and the sociogenetic organization of colonies. The polygyny-vs.-polyandry hypothesis argues that polygyny and polyandry should be negatively associated since both can result in increased intracolonial genetic variability and have costs. However, evidence for this long-debated hypothesis has been lacking at the intraspecific level. Ants of the genus Myrmecia Fabricius display many ancestral biological traits, and thus are considered valuable in investigating the origin and evolution of more derived social behaviors, life histories and morphologies as found in other ants. In this research, a set of highly polymorphic microsatellite loci were developed, and employed to determine fine-scale sociogenetic organizations in two species of this genus, i.e., the bulldog ant M. brevinoda and the jumper ant M. pilosula. The polygyny-vs.-polyandry hypothesis was also examined using both cases. In addition, I evaluated nestmate recognition in M. brevinoda using behavioural assays, and investigated the impacts of colony social structure, genetic and spatial distances on recognition and aggression. M. brevinoda is facultatively polygynous and polyandrous. The numbers of queens per colony varied from 1 to 6, and queens were inferred to mate with 1 to 10 males. Nestmate queens within polygynous colonies were on average related, but the overall relatedness between queens and their mates was indistinguishable from zero. A lack of genetic isolation by distance among nests indicated the prevalence of independent colony foundation. In accordance with the polygyny-vs.-polyandry hypothesis, the number of queens per colony was significantly negatively associated with the estimated number of matings (Spearman rank correlation R = -0.490, P = 0.028). This study thus provides the rare intraspecific evidence for the polygyny-vs.-polyandry hypothesis.. vi.
(13) Workers of M. brevinoda were always non-aggressive towards nestmates, but acted either aggressively or non-aggressively towards alien conspecifics, suggesting that they are generally able to discriminate between nestmates and non-nestmates. Mantel tests revealed no significant impact of genetic and spatial distances on nestmate discrimination. Moreover, the data appear to lend no support to the hypothesis that colony social structure (queen number) variation significantly affects nestmate recognition and aggression. Thus, the actual mechanism underlying nestmate recognition in this species remains to be resolved. M. pilosula is also facultatively polygynous and polyandrous. The number of queens per colony ranged from 1 to 4, and queens were inferred to mate with 1-9 males. Nestmate queens within polygynous colonies, and queens and their mates, were generally unrelated. This is the first time that the rare co-occurrence of polygyny and high polyandry has been found in the M. pilosula species group. The isolation-by-distance pattern and the occurrence of polygynous polydomy suggest the occurrence of dependent colony foundation in M. pilosula; however, independent colony foundation may co-occur since queens of this species have fully developed wings and can fly. There is no support for the predicted negative association between polygyny and polyandry in ants. Combining the support from the case of M. brevinoda and the rejective evidence from the case of M. pilosula and other intraspecific studies, I suggest that the high costs of multiple matings and the strong effect of multiple matings on intracolonial genetic diversity may be essential to the negative association between polygyny and polyandry, and that any attempt to empirically test this hypothesis should place emphasis upon these two key underlying aspects.. vii.
(14)
Related documents
Since 1986 Australian organisations (greater than 100 employees in size) have been writing and submitting annual and later, biennial progress reports on the equal opportunities of
During the treatment phase of the reciprocity condition, the mate of the focal subject had access to the handle of an out-of-reach tray that, when pulled, provided a small food
While spring phenology in temperate deciduous forests has been extensively studied in southern New England, Northern Maine is comparatively much less developed, closer to
Aedeagus: dorsal side with long thin incision separating slightly wider and longer left part with wider apex from narrower and shorter right part with subtriangular apex; ventral side
Integrated logistic solutions for support to State NG organizations, State EMO’s, the local Red Cross and VOADs: To assist the communities needs. STATE NG Stockpile State EMO
Microfinance banks since inception have existed for more than 10 years in Nigeria, hence, they have exerted some effects on the economic activities of the rural small
1945, pp. Ruling out such inherently fallacious schemes leaves the remaining valid ones. These fall into two categories. The second includes activist feedback rules
This, combined with the norms of Tumblr following in which users connect through shared interests with a decreased pressure to follow people they know offline, means that
