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Social Polymorphism and Dispersal in Formica Ants

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Social Polymorphism and Dispersal in Formica Ants Faculty of Biological and Environmental Sciences SANJA HAKALA University of Helsinki Social polymorphism and SOCIAL POLYMORPHISM AND DISPERSAL IN SOCIAL POLYMORPHISM dispersal in Formica ants SANJA MARIA HAKALA FORMICA ANTS 2020 ISBN 978-951-51-5972-4 Social polymorphism and dispersal in Formica ants SANJA MARIA HAKALA Organismal and evolutionary biology research programme Faculty of Biological and Environmental Sciences University of Helsinki Tvärminne Zoological Station University of Helsinki ACADEMIC DISSERTATION To be presented for public examination with the permission of the Faculty of Biological and Environmental Sciences of the University of Helsinki in Metsätalo room 2 (Unioninkatu 40), on June 9th at 12.00 o’clock noon. HELSINKI 2020 SUPERVISORS: Dr. docent Heikki Helanterä Ecology and genetics research unit University of Oulu Dr. docent Perttu Seppä Organismal and evolutionary biology research programme University of Helsinki REVIEWERS: Prof Heike Feldhaar Faculty for Biology, Chemistry, and Earth Sciences University of Bayreuth Dr. docent Kristjan Niitepõld University of Helsinki / Heureka, the Finnish Science Centre OPPONENT: Prof Mark Brown Department of Biological Sciences Royal Holloway, University of London CUSTOS: Prof Liselotte Sundström Organismal and evolutionary biology research programme University of Helsinki MEMBERS OF THESIS ADVISORY COMMITTEE: Dr. docent Marjo Saastamoinen Organismal and evolutionary biology research programme University of Helsinki Dr. docent Riitta Savolainen Organismal and evolutionary biology research programme University of Helsinki Summary © Sanja Hakala, CC BY 4.0 Chapters I, II and IV © The authors and the publishers, CC BY 4.0 Chapter III © The authors Cover illustration © I. Hakala, O. Hakala, S. Hakala, Other illustrations © J. Beresford, C. Elgert, I. Hakala, K. Kyrö, S. Sinisalo, A. Tilquin, M. Tiusanen Layout Sanja Hakala, Sami Ojanen ISBN 978-951-51-5972-4 (Print) ISBN 978-951-51-5973-1 (PDF) http://ethesis.helsinki.fi Painosalama oy, Turku 2020 Kuule istuta vielä se omenapuu vaikka tuli jo tukkaasi nuolee vaikka huomenna saaste jo laskeutuu vaikka huomenna aurinko kuolee Juice Leskinen (1981) CONTENTS / SISÄLLYS ABSTRACT 6 TIIVISTELMÄ 7 SUMMARY 8 1 INTRODUCTION .................................................................................................................................. 8 2 AIMS OF THE THESIS ......................................................................................................................12 3 METHODS ...........................................................................................................................................13 4 MAIN RESULTS AND DISCUSSION ..............................................................................................18 5 CONCLUSIONS AND FUTURE DIRECTIONS ..............................................................................23 6 ACKNOWLEDGEMENTS ..................................................................................................................25 7 REFERENCES ......................................................................................................................................28 CHAPTER I * 35 CHAPTER II * 59 CHAPTER III * 85 CHAPTER IV * 119 * Jokainen kappale alkaa suomenkielisellä tiivistelmällä. Every chapter begins with a Finnish translation of its abstract. LIST OF ORIGINAL PUBLICATIONS The thesis is based on the following articles, which are referred to in the text by their Roman numerals: I Hakala, S., Seppä, P., Helanterä, H. “Evolution of dispersal in ants (Hymenoptera: Formicidae): a review on the dispersal strategies of sessile superorganisms”, Myrmecological News 2019, 29: 35-55. II Hakala, S., Seppä, P., Heikkilä, M., Punttila, P., Sorvari, J., Helanterä, H. “Genetic analysis reveals Finnish Formica fennica populations do not form a separate genetic entity from F. exsecta”, PeerJ 2018, 6:e6013. III Hakala, S., Belevich, I., Jokitalo, E., Seppä, P., Helanterä, H. ”Social polymorphism in Formica ants is a result of dispersal behavior rather than dispersal morphology”, manuscript. IV Hakala, S.*, Ittonen, M.*, Seppä, P., Helanterä, H. “Limited dispersal and unexpected aggression in a native supercolonial ant”, Ecology and Evolution 2020, 00:1–15. * These authors contributed equally to the manuscript Authors' contribution in each chapter of this thesis: I II III IV Original idea SH HH, PS SH, HH SH, MI, HH, PS Design SH HH, PS, SH SH, HH, PS, EJ SH, MI, HH, PS Data Collection - HH, PS, JS, PP SH MI Analyses - SH, PP, JS, MH SH, IB SH, MI Manuscript preparation SH, HH, PS SH, HH, PS, PP, MH, JS SH, HH, PS, IB, EJ SH, MI, HH, PS EJ=Eija Jokitalo, HH=Heikki Helanterä, IB=Ilya Belevich, JS=Jouni Sorvari, MH=Maria Heikkilä, MI=Mats Ittonen, PP=Pekka Punttila, PS=Perttu Seppä, SH=Sanja Hakala In addition to the authors listed here, Heini Ali-Kovero, Hanne Henrikson, Leena Laaksonen, Mervi Lindman and Arja Strandell provided invaluable technical assistance with the samples in projects II, III and IV. © MIKKO TIUSANEN ABSTRACT ABSTRACT There are intricate links between the evolution by their morphology or resources the individuals get of sociality and the spatial population structures from their natal colonies. The traits of all species and created by dispersal. In ants, the evolution of the both sexes indicate good flight ability, with overall male most complex societies, supercolonies, is strongly bias and large variation both among and within species. connected to limited dispersal. The supercolonies The increased philopatry in supercolonial species and consist of hundreds of interconnected nests where populations is more a behavior change: the queens are thousands of queens and their workers cooperate over philopatric even though the society provides them large areas. Supercolonies arise from simpler family resources for dispersal. However, I observed a small units when large proportions of daughter queens are decrease of male flight muscle ratio in supercolonial philopatric and stay in their natal colony as additional species, which indicates strong coevolution of the reproducing queens instead of dispersing by wing. This sexes. allows the colonies to grow quickly and colonize large areas, but also increases social conflicts due to very In order to better understand the outcomes of low local relatedness in these societies. limited dispersal in supercolonial Formica, I analyzed the behavioral and genetic structure of a dense In this thesis I inspect the evolution and maintenance supercolonial population of Formica pressilabris. The of ant supercolonies, by focusing on dispersal traits and population is genetically viscous at a small spatial the consequences of dispersal in socially polymorphic scale, but still not genetically structured by location Formica ants. Formica have both simple family-based on a larger spatial scale. This indicates that although monodomous colonies and complex supercolonies, dispersal is limited within the population, a large and some species have also intraspecific variation. To enough proportion of individuals do disperse to keep lay a sound theoretical background for my work, I the local populations connected. Interestingly, when began by synthesizing current knowledge of dispersal analyzing worker behavior among the polydomous evolution in ants. In my literature review I showed nests, the observed aggression pattern indicates that how eco-evolutionary feedbacks link the evolution they are not a single cooperative unit – but also not of ant dispersal strategies and social organization, clearly separate colonies. The sensitive behavioral and pinpointed the most relevant future research assay developed for this study shows that workers directions. Next, to be able to inspect some of the allow a proportion of individuals from outside nests hypotheses formulated in the review, I clarified the to enter their own nest material, but are slightly more species identification of one of my intended study aggressive towards individuals from further away. This species, Formica fennica with molecular methods, and indicates the population is only partially cooperative concluded that the populations I studied should be over the whole nest aggregation, and shows that the treated as conspecific to Formica exsecta. inner structures of supercolonies should be analyzed in more detail. I analyzed the individual dispersal traits of six socially variable species of Formica ants to assess whether This thesis sheds light on ants’ dispersal ability and dispersal ability varies between monodomous and behavior, and demonstrates the crucial role of dispersal supercolonial societies in accordance to the observed in the evolution of their different social structures. My behavioral difference. According to my results the results also raise new questions about possible conflicts dispersal behavior of these species is likely not restricted over dispersal in ant societies. 6 TIIVISTELMÄ TIIVISTELMÄ Sosiaalisuuden evoluutio linkittyy vahvasti siihen, kuinka Jokaisen tutkimani lajin ominaisuudet viittaavat siihen, eliöt hajaantuvat elinympäristöönsä levittäytymisen että sekä koiraat että kuningattaret osaavat lentää hyvin. seurauksena. Muurahaisten monimutkaisimpien yhteis- Koirailla on parempi lentokyky kuin kuningattarilla, ja kuntien, superkolonioiden, evoluutio on yhteydessä sekä lajien välillä että lajien sisällä yksilöiden välillä rajoittuneeseen levittäytymiseen. Superkoloniat on suurta vaihtelua. Se, että superkoloniaalisten koostuvat
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