'Safer without Sex?' Thelytokous Parthenogenesis and Regulation of Reproduction in the Ant Platythyrea punctata Dissertation at the Julius-Maximilians-University Würzburg submitted by Klaus Schilder Bremen Würzburg, 1999 Erklärung: Hiermit erkläre ich ehrenwörtlich, dass die vorliegende Dissertation von mir selbständig und nur unter Verwendung der angegebenen Quellen und Hilfsmittel angefertigt wurde. Diese Dissertation wurde weder in gleicher noch in ähnlicher Form in einem anderen Prüfungsverfahren vorgelegt. Des weiteren erkläre ich, dass ich früher weder akademische Grade erworben noch zu erwerben versucht habe. Eingereicht am: ................................................................................ Mitglieder der Promotionskommission: Vorsitzender: .................................................................................... 1. Gutachter : Prof. Dr. Bert Hölldobler 2. Gutachter: Prof. Dr. Jürgen Heinze Tag des Promotionskolloquiums: ...................................................... Doktorurkunde ausgehändigt am: ...................................................... Acknowledgements First of all, I would like to express my thanks to Prof. Dr. Jürgen Heinze for his encouragement to pursue the ways of the ant Platythyrea punctata, for his support during all stages of the work, for discussions and ideas, as well as detailed comments and suggestions on manuscripts and on the dissertation. His support enabled me to travel twice to Florida and Puerto Rico to work in the natural habitat of this fascinating ant. Similarly, I'm thankful to Prof. Dr. Bert Hölldobler for his support during all stages of the research. In his department he provided excellent facilities and a lively scientific atmosphere that made this research possible. During my field work in Florida and Puerto Rico, Mark Deyrup, Lloyd Davis and Juan Torres provided invaluable advise on the natural history of the species. Both Dr. Jürgen Gadau and Olav Rüppell did a great job in helping to collect P. punctata and keeping company. Many thanks are due to Prof. Dr. Roy Gross for providing facilities to develop microsatellites at the Department of Microbiology. Thilo, Jochen, Heike and Barbara patiently answered all my molecular-biological questions and were great fun to work with in the lab. Thanks to Klaus and Indrajit, Department of Human Genetics, for help with karyotype analysis. Thanks for fruitful scientific discussions to Kasuki Tsuji, Pia Gertsch, Stan Braude and Michael Haberl. Of course, I would like to thank all my colleagues at the Department of Zoology II for help in many aspects of the work, for good company and friendship. Thanks, Corinna, Jürgen, Jürgen, Olav, Diethe, Brigitte, Anja, Christoph, Johannes, Annette, Roman, Flavio and Uli. Finally, I would especially like to thank my parents for their patience, understanding and support not only during my dissertation, but during my whole academic career. For my parents Contents l v Contents 1 Introduction................................................................................. 8 2 Life history traits ......................................................................12 2.1 Introduction............................................................................12 2.2 Material and methods .............................................................17 2.3 Distribution and habitat ..........................................................20 2.4 Composition of colonies..........................................................24 2.5 Morphology ...........................................................................24 2.6 Nestmate recognition ..............................................................28 2.7 Division of labor ....................................................................29 2.8 Discussion..............................................................................31 3 Reproductive regulation........................................................38 3.1 Introduction............................................................................38 3.2 Material and methods .............................................................43 3.2.1 Colony dissection................................................43 3.2.2 Experimental worker groups ...............................43 3.2.3 Behavioral observations................................................44 3.3 Results...................................................................................48 3.3.1 Partitioning of reproduction ................................48 3.3.2 Thelytokous parthenogenesis...............................49 3.3.3 Reproductive regulation in worker groups ...........52 Contents l vi 3.4 Discussion..............................................................................74 4 Genetic population structure...............................................84 4.1 Introduction............................................................................84 4.2 Material and methods .............................................................88 4.2.1 Study sites and specimens ...................................88 4.2.2 DNA extraction ..................................................88 4.2.3 Construction of partial genomic library ...............89 4.2.4 Microsatellite identification and sequencing.........89 4.2.5 PCR analysis......................................................90 4.2.6 Data analysis......................................................91 4.2.7 Chromosome preparation .....................................91 4.3 Results...................................................................................92 4.3.1 Microsatellite marker loci ...................................92 4.3.2 Intra - population survey.....................................94 4.3.3 Inter - population survey .....................................95 4.3.4 Cross - species amplification...............................95 4.3.5 Karyotype...........................................................97 4.4 Discussion..............................................................................98 5 Evolution of thelytoky among the Hymenoptera ...........................................................................104 5.1 Introduction..........................................................................104 5.2 Thelytokous parthenogenesis in the Hymenoptera..................104 5.3 Mechanisms of thelytokous parthenogenesis..........................109 5.3.1 Genetic origin of thelytoky ................................109 5.3.2 Bacteria as causing agents ................................112 Contents l vii 5.3.3 Hybrid origin....................................................113 5.4 The ecology of thelytoky.......................................................114 5.5 When to have sex?................................................................115 5.6 Hopeful monsters or transposon mutations? ..........................116 5.7 Why is thelytoky rare?..........................................................118 5.8 Conclusions..........................................................................119 6 General discussion ...............................................................120 7 Summary ...................................................................................127 8 Zusammenfassung ................................................................130 9 References ...............................................................................134 10 Abbreviations ..........................................................................146 11 Annex .........................................................................................147 12 Publications .............................................................................159 13 Curriculum vitae .....................................................................160 Front cover: Drawing of Platythyrea parallela after Wilson and Taylor 1967. Introduction l 8 1 Introduction Ants are everywhere (Hölldobler and Wilson 1990). They probably evolved some 100-130 million years ago (Agosti et al. 1998) and subsequently have been remarkably successful across a broad range of habitats. Being eusocial (truly social), ants show some of the most complex social organizations currently known. Most of the colony members have given up own reproduction in favor of helping nestmates to rear their offspring. The evolution of altruism is the central problem underlying the evolution of eusociality (Trivers 1971; Alexander 1974; West-Eberhard 1975; Gadagkar 1994). Wilson (1971) defined eusociality as the possession of all of the following traits: a) cooperative brood care of conspecifics, b) reproductive division of labor with sterile or subfertile individuals working on behalf of fecund individuals, and c) overlap of generations with offspring helping their parents. In addition to the eusocial Hymenoptera (ants, bees and wasps) and Isoptera (termites), within the last years eusociality has been found in aphids (Aoki 1977; Ito 1989), ambrosia beetles (Kent and Simpson 1992), thrips (Crespi 1992), possibly in spiders (Vollrath 1986), in shrimps (Duffy 1996) and in several naked mole rats (Jarvis 1981; Sherman et al. 1991; Burda and Kawalika 1993). Within the Hymenoptera alone, eusociality evolved several times, possibly as often as 12 times (Wilson 1971). Since eusociality also evolved several times independently within aphids and naked mole-rats (Jarvis et al. 1994; Stern 1994), the phenomenon is not such a rare evolutionary achievement as it was once perceived (Hölldobler