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Behavioural Genetics of the Leaf-Cutting Ant Acromyrmex Echinatior

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Behavioural Genetics of the Leaf-Cutting Ant Acromyrmex Echinatior faculty of science university of copenhagen Behavioural Genetics of the Leaf-Cutting Ant Acromyrmex echinatior Jack Howe MSc Thesis: 60 ETCS Academic Supervisors: Jacobus J Boomsma and Morten Schiøtt Centre of Social Evolution, University of Copenhagen September 2015 Danish National Research Foundation Centre for Social Evolution Preface This work is submitted to fulfil the requirements for a 60 ECTS thesis for the completion of the MSc in Biology at the University of Copenhagen. It marks the completion of 12 months of work under the supervision of Associate Professor Morten Schiøtt and Professor Jacobus J. Boomsma at the Centre for Social Evolution (CSE). A total of 1 month was spent at the Smithsonian Tropical Research Institute, in Gamboa, Panama. This work consists of three chapters, covering a range of topics within social evolu- tion: genomic imprinting, the division of labour and symbiont transmission. Each chapter represents an independent line of research, and each is presented in turn, following an in- troduction that provides a brief background and justification of each. The first chapter presents work conducted in collaboration with Qiye Li and Zongji Wang of the Beijing Genomics Institute (BGI), who kindly granted me access to the remarkable data set that was used as the foundation of this chapter. Some of the data that are presented in chap- ter 2 have previously submitted for the completion of a 7.5ECTS speciale-projekt in 2014. Sufficient new data have been added, in the form of two further experiments, that it is submitted again here as part of a larger thesis. These data were also presented as a poster at the 2015 ESEB conference held in Lausanne in August 2015, this poster is included at the end of the thesis. The third chapter is based on work conducted during a two week period in Gamboa, Panama during May of 2015. Finally, I discuss the questions arising from this work, and potential avenues of future study. The work of each chapter is ongoing, and each will contribute to either manuscripts to be submitted for review in the near future, or will form the basis of work to be completed over the course of a PhD commencing Fall 2015. The cover photo was taken by David Nash. Contents General Abstract i List of Figures ii List of Tables iv Introduction 1 0.1 BehaviouralGeneticsintheSocialInsects . 1 0.2 TheAttineAntsasaModelSystem. 4 0.3 Conflict and Imprinting in Insect Societies . 6 0.4 The Self-Organisation of Insect Colonies . 9 0.5 Ant-FungusSymbiosis .............................. 11 1 The Use of Transcriptomic Data to Identify Imprinted Genes in Social Insects 27 1.1 Whole-GenomeSearchesUsingTranscriptomics . 32 1.2 Application to Acromyrmex echinatior ..................... 38 1.2.1 Methods . 39 1.2.2 Results . 45 1.2.3 Discussion . 49 Figures....................................... 54 Appendices 61 2 A Potential Role for the Neuropeptide Tachykinin in Acromyrmex echi- natior Division of Labour 77 2.1 Methods . 84 2.2 Results . 90 2.3 Discussion . 94 Figures....................................... 100 3 Horizontal Transfer of a Leaf-Cutting Ant’s Fungal Symbiont In Situ 119 3.1 Methods . 123 3.2 Results . 124 3.3 Discussion . 126 Figures....................................... 129 Conclusions and Future Directions 134 ESEB Poster 2015 140 Acknowledgements 141 General Abstract The fungus-growing ant Acromyrmex echinatior is increasingly being used as a model species for the study of social evolution owing to its obligate association with a symbi- otic fungus and a range of bacteria, its complicated colony kin-structure and caste system, and the increasing availability of genetic data. I utilised this data to explore three evolu- tionary questions. First, I conducted the first genome-wide survey for genomic imprinting in an ant, and developed novel techniques to search for imprinting in previously intractable species. Although this search has been unsuccessful so far, a number of candidate genes have been identified that warrant further study, and the techniques developed may aid in the search for imprinted genes in the social insects. Second, I tested for the role of tachykinin, a neuropeptide-encoding gene, in the aggressive division of labour within a colony. I com- pared behaviour and gene expression among the various worker castes and in various stages of the reproductive females. I also manipulated the aggression of virgin queens and tested for changes in gene expression. Expression patterns suggest that tachykinin may play a role in the division of labour, at least in the worker castes, but there are inconsistencies in the reproductive caste. Finally, the fortunate discovery of clusters of very young A. echinatior colonies, in a stage where the queen is still foraging, enabled a test for horizontal transmis- sion of the fungal symbiont in a natural setting. This work demonstrated that young A. echinatior queens will search for and adopt novel symbiont fungal symbionts after the loss of their own. i List of Figures 1.1 PredictionsofASEUnderGenomicImprinting. 54 1.2 PredictionsofASEwithVaryingQueenGenotypes . 55 1.3 Allele Specific Expression of Vitellogenin 1 : GenomeWideData . 56 1.4 Allele Specific Expression of Major Royal Jelly Protein III : Genome Wide Data........................................ 57 1.5 Allele Specific Expression of Major Royal Jelly Protein III: ddPCR Data . 58 1.6 Allele Ratios for Major Royal Jelly Protein III: Pooled Male DNA . 59 1.7 Allele Ratios for Major Royal Jelly Protein III: Individual Male DNA . 60 2.1 Aggression of A. echinatior Castes . 100 2.2 Expression levels of Tachykinin and Tachykinin-Receptor 99D . 101 2.3 Relationship Between Tachykinin and Tachykinin-Receptor 99D Expression . 102 2.4 Brain Allometry of A. echinatior Castes . 103 2.5 Brain-Size Corrected Expression Levels . 104 2.6 Worker-likeBehaviourofWinglessVirginQueens . 105 2.7 Expression of Tac and TacR99D After Wing-Clipping . 106 3.1 An Acromyrmex echinatior queen with her nascent fungus garden . 119 3.2 FungusStealing:SiteA ............................. 129 ii 3.3 Fungus Stealing: Site B . 130 3.4 TheE↵ect of Distance on Stealing Fungus Vs. Relocating . 131 iii List of Tables 1 GeneswithSignificantASE ........................... 61 2LociConsistentwithImprinting.........................63 iv Introduction Ants are so much like human beings as to be an embarrassment. They farm fungi, raise aphids as livestock, launch armies into war, use chemical sprays to alarm and confuse enemies, capture slaves, engage in child labour, exchange information ceaselessly. They do everything but watch television. The Lives of a Cell, Lewis Thomas, 1974 0.1 Behavioural Genetics in the Social In- sects In the past decade or so, several fields of social biology have begun to converge upon genetics (Johnson and Linksvayer, 2010; Robinson et al., 2005). As the fundamental unit of evolution (Dawkins, 1976), it is perhaps not surprising that the gene is receiving so much attention, but up until very recently, the genetic underpinnings of traits were only really the purview of those of those working with the few model organisms for which there was sufficient genomic data: Drosophila, Mus,orCaenorhabditis. With the precipitous decline in the cost of DNA-sequencing (Sboner et al., 2011), attention is now being turned to the complex societies of the social insects, attempting to decipher the molecular basis of their social organisation, and to determine the e↵ects of colony life on the genome (Robinson et al., 2005). There are two broad methods applied in the search of genetic e↵ects on behaviour, which of the two is applied depends on the availability of genomic data for the organism 1 under study, and its experimental tractability (Oldroyd and Thompson, 2006). The reverse- genetics approach tests the role of few candidate genes with known functions from model organisms in novel systems (Fitzpatrick et al., 2005). In contrast, a forward-genetics ap- proach requires no such prior knowledge. Forward-genetic approaches test as many genes as possible throughout the genome to identify candidate genes. This has been, until recently, limited to species that can be bred in the lab, or can be subject to mutagenesis screens (Ol- droyd and Thompson, 2006). Now however, high-throughput sequencing is making many more organisms accessible to forward-genetic approaches, radically changing the field of behavioural genetics (Gadau et al., 2012; Libbrecht et al., 2013; Schneeberger and Weigel, 2011) Of the two techniques, the candidate gene approach has been the most successful in the social insects, and a number of genes have been identified with roles in caste determination, and the division of labour in particular. The candidate gene approach is dependent on the conservation of genes across taxa; that social behaviours are encoded by genes that con- trol similar phenotypes in other, better-studied organisms (Fitzpatrick et al., 2005). The identification of the protein-kinase encoded by the forager gene in the foraging behaviour of Drosophila and the honeybee have become a paradigmatic example of the application of reverse-genetics in the social insects. Two distinct foraging phenotypes were identified in Drosophila larvae: those that moved relatively little, and those that left long foraging trails. Careful breeding first narrowed the gene responsible for this down to chromosome 2 (Sokolowski, 1980), and subsequent mutagenesis screens identified the responsible gene as a cGMP-dependent Protein Kinase (Osborne et al., 1997). Targeted measurements of honey- bee
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