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The Importance of Recognition and Aggression in the Coevolution Between Ant Social Parasites and Their Hosts

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The Importance of Recognition and Aggression in the Coevolution Between Ant Social Parasites and Their Hosts The importance of recognition and aggression in the coevolution between ant social parasites and their hosts Dissertation Zur Erlangung des Grades Doktor der Naturwissenschaften Am Fachbereich Biologie Der Johannes-Gutenberg Universität Mainz Isabelle Kleeberg geb. am 02.06.1986 in Hildesheim Mainz, 2016 Dekan: Herr Prof. Dr. Hans Zischler 1. Berichterstatterin: Frau Prof. Dr. Susanne Foitzik 2. Berichterstatter: Herr Prof. Dr. Thomas Schmitt Tag der mündlichen Prüfung: 20.05.2016 „A truly successful parasite is commensal, living in amity with its host, or even giving it positive advantages. A parasite that regularly and inevitably kills it hosts cannot survive long, in the evolutionary sense, unless it multiplies with tremendous rapidity. It is not pro-survival. Mr. Spock, Star Trek 2 This thesis is based on the following seven research articles, which are presented as chapters 1 – 7 and referred to in the general introduction and discussion by their respective number: 1. Kleeberg I, Pamminger T, Jongepier E, Papenhagen M & Foitzik S (2014) Forewarned is forearmed: aggression and information use determine fitness costs of slave raids. Behavioral Ecology 25: 1058 – 1063. 2. Kleeberg I, Jongepier E, Job S & Foitzik S (2015) Geographic variation in parasite pressure predicts intraspecific but not interspecific aggressive responses in hosts of a slavemaking ant. Ethology 121: 1 – 9. 3. Jongepier E, Kleeberg I, Job S & Foitzik S (2014) Collective defense portfolios of ant hosts shift with social parasite pressure. Proceedings of the Royal Society of London B: Biological Sciences 281: 20140225. 4. Jongepier E, Kleeberg I & Foitzik S (2015) The ecological success of a social parasite increases with manipulation of collective host behavior. Journal of Evolutionary Biology 28: 2152 – 2162. 5. Seifert B, Kleeberg I, Feldmeyer B, Pamminger T, Jongepier E & Foitzik S (2014) Temnothorax pilagens sp. n. - a new slavemaking species of the tribe Formicoxenini from North America (Hymenoptera, Formicidae). ZooKeys 368: 65 – 77. 6. Kleeberg I & Foitzik S (2016) The placid slavemaker: avoiding detection and conflict as an alternative, peaceful raiding strategy. Behavioural Ecology and Sociobiology 70: 27 – 39. 7. Kleeberg I, Menzel F & Foitzik S. The evolution of cuticular hydrocarbons in ants: The influence of parasitic lifestyle, caste and sex on chemical profiles. Submitted to Evolution. TABLE OF CONTENTS Summary ................................................................................................................................... 1 Zusammenfassung ................................................................................................................... 2 General Introduction .............................................................................................................. 4 Chapter 1: Forewarned is forearmed: aggression and information use determine fitness costs of slave raids .................................................................................................. 14 Chapter 2: Geographic variation in parasite pressure predicts intraspecific but not interspecific aggressive responses in hosts of a slavemaking ant ............................. 25 Chapter 3: Collective defense portfolios of ant hosts shift with social parasite pressure .................................................................................................................................. 39 Chapter 4: The ecological success of a social parasite increases with manipulation of collective host behavior .................................................................................................. 56 Chapter 5: Temnothorax pilagens sp. n. - a new slavemaking species of the tribe Formicoxenini from North America (Hymenoptera, Formicidae) ............................. 72 Chapter 6: The placid slavemaker: avoiding detection and conflict as an alternative, peaceful raiding strategy .............................................................................. 86 Chapter 7: The evolution of cuticular hydrocarbons in ants: The influence of parasitic lifestyle, caste and sex on chemical profiles ................................................ 113 General Discussion ............................................................................................................. 142 References ............................................................................................................................ 151 Lebenslauf ............................................................................................................................ 177 SUMMARY In my dissertation I investigate host defense and parasite offense strategies in different species of Temnothorax slavemaking ants (social parasites) and their hosts. The thesis is mainly divided into two parts: (1) The evolution of host defense behaviors in relation to parasite pressure and (2) The evolution of slavemaker counter-adaptations. Temnothorax host colonies are able to recognize the slavemaker T. americanus as a threat and respond with high aggression towards it. During raids, having recent contact with a slavemaker worker yields fitness benefits, but only for those colonies that have a high aggressive potential. Hence, Temnothorax hosts are able to utilize information of an upcoming attack to better defend themselves, when being aggressive (Chapter 1). But this was only true for aggression towards conspecifics – baseline aggression - which was moreover positively related to parasite abundance in a population. This indicates that parasites select for more aggressive host colonies. The correlation was found for two host species of T. americanus, pointing to convergent evolution of aggression as a defense strategy (Chapter 2). Aggression towards a living and potentially manipulative parasite decreased with parasite pressure, instead host colonies switched to an alternative defense mechanism – evacuation (Chapter 3). Populations that were less aggressive towards the parasite were also less resistant to chemical manipulation and slavemakers benefitted from it, as the likelihood of parasite survival and the parasites abundance increased (Chapter 4). One of the three slavemaker species evolved a different strategy – chemical camouflage – to steal adult host ants, known as eudulosis (Chapter 5-6). Hosts of this slavemaker do recognize the two slavemaker species T. americanus and T. duloticus, but are unable to identify their sympatric slavemaker T. pilagens. However, if they do recognize the slavemaker, aggression is costly as most workers die during raids, and evacuation although utilized in confrontations with T. americanus, seems to not be employed during raids of T. pilagens (Chapter 6). The three slavemaker species, although of different evolutionary origin, moreover show convergent evolution of a specific chemical profile that may undermine host recognition (Chapter 7). We detected an intricate suite of adaptations and counter-adaptations in Temnothorax hosts and slavemakers. I aimed to shed light on the diverse roles of recognition and aggression within this system and found evidence for convergent evolution of both, possibly due to their similar lifestyles of slavemakers and hosts, respectively. Studying different host populations with differences in reciprocal selection, based on variation in parasite abundance, allowed for the elucidation of the selective forces that shape host behavior. Comparing different slavemaker species within the same genus, each representing different origins of slavery and evolutionary age, moreover allows delineating trends in the evolution of parasitic lifestyle. 1 ZUSAMMENFASSUNG Wirt-Parasit Interaktionen zählen du den stärksten Kräften der Evolution, da dabei der Parasit die Fitness des Wirtes negativ beeinflussen kann. Dies führt zu gegenseitigen evolutionären Änderungen durch natürliche Selektion – Koevolution. In meiner Dissertation untersuchte ich die Auswirkungen von Parasitismus auf das Verteidigungsverhalten von Wirten und umgekehrt die Evolution von Angriffststrategien bei Parasiten. Sklavenhaltende Ameisen sind Sozialparasiten, die Ameisenkolonien einer andern Art ausrauben, um deren Brut (zukünftige Sklaven) zu stehlen. Hier untersuchte ich zum Einen die Fähigkeit den Parasiten zu erkennen bzw. die Fähigkeit des Parasiten die Feinderkennung zu unterbinden. Zum Anderen untersuchte ich inwiefern aggressives Verhalten von Wirtskolonien Fitness Vorteile bringt, und ob dies Verhalten unter Selektion des Parasiten steht. Temnothorax Wirtskolonien können den Sklavenhalter als Gefahr erkennen und reagieren entsprechend mit erhöhter Aggression. Wirtskolonien die kürzlich Kontakt zu einer Sklavenhalterin hatten und überdies ein hohes aggressives Potential aufweisten, konnten mehr Brut retten. Dies deutet darauf hin, dass Wirtskolonien in der Lage sind, Informationen über einen anstehenden Raubzug zu nutzen, um sich besser zu verteidigen (Kapitel 1). Außerdem lässt dies vermuten, dass Sklavenhalter Wirtskolonien mit einem hohen aggressiven Potential selektieren und in der Tat konnte dies gezeigt werden. Wirtspopulationen die einem hohen Parasitedruck ausgesetzt waren, wiesen auch ein hohes aggressive Potential aus. Dieser Zusammenhang konnte in zwei Wirtsarten gezeigt werden, was auf konvergente Evolution als Antwort auf den Parasitendruck hindeutet (Kapitel 2). Die Aggression gegenüber eines Sklavenhalters, der zudem in der Lage ist die Wirte chemisch zu seinem eigenen Vorteil zu manipulieren, war geringer in Populationen
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