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Mechanisms for the Evolution of Superorganismality in Ants

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Mechanisms for the Evolution of Superorganismality in Ants Rockefeller University Digital Commons @ RU Student Theses and Dissertations 2021 Mechanisms for the Evolution of Superorganismality in Ants Vikram Chandra Follow this and additional works at: https://digitalcommons.rockefeller.edu/ student_theses_and_dissertations Part of the Life Sciences Commons MECHANISMS FOR THE EVOLUTION OF SUPERORGANISMALITY IN ANTS A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy by Vikram Chandra June 2021 © Copyright by Vikram Chandra 2021 MECHANISMS FOR THE EVOLUTION OF SUPERORGANISMALITY IN ANTS Vikram Chandra, Ph.D. The Rockefeller University 2021 Ant colonies appear to behave as superorganisms; they exhibit very high levels of within-colony cooperation, and very low levels of within-colony conflict. The evolution of such superorganismality has occurred multiple times across the animal phylogeny, and indeed, origins of multicellularity represent the same evolutionary process. Understanding the origin and elaboration of superorganismality is a major focus of research in evolutionary biology. Although much is known about the ultimate factors that permit the evolution and persistence of superorganisms, we know relatively little about how they evolve. One limiting factor to the study of superorganismality is the difficulty of conducting manipulative experiments in social insect colonies. Recent work on establishing the clonal raider ant, Ooceraea biroi, as a tractable laboratory model, has helped alleviate this difficulty. In this dissertation, I study the proximate evolution of superorganismality in ants. Using focussed mechanistic experiments in O. biroi, in combination with comparative work from other ant species, I study three major aspects of ant social behaviour that provide insight into the origin, maintenance, and elaboration of superorganismality. First, I ask how ants evolved to live in colonies, and how they evolved a reproductive division of labour. A comparative transcriptomic screen across the ant phylogeny, combined with experimental manipulations in O. biroi, finds that reproductive ants have higher insulin levels than their non-reproductive nestmates, and that this likely regulates the reproductive division of labour. Using these data, as well as studies of the idiosyncrasies of O. biroi’s life history, I propose a mechanism for the evolution of the first colonies. It is possible that similar mechanisms underlie the evolution of reproductive division of labour in other superorganisms, and of germ-soma separation in nascent multicellular individuals. Second, I ask how ant workers assess colony hunger to regulate their foraging behaviour. I find that workers use larval signals, but not their own nutritional states, to decide how much to forage. In contrast, they use their nutritional states, but not larval signals, to decide how much to eat, suggesting that in at least some ant species, foraging and feeding have been decoupled. This evolution of colony-level foraging regulation has occurred convergently in hymenopteran superorganisms, and is analogous to the evolution of centralised regulation of foraging behaviour in multicellular animals. Finally, I ask how an iconic collective foraging behaviour – the mass raids of army ants – evolved. I find that O. biroi, a relative of army ants, forages collectively in group raids, that these are ancestral to the mass raids of army ants, and that the transition from group to mass raiding correlates with expansion in colony size. I propose that the scaling effects of increasing colony size explain this transition. It is possible that similar principles underlie the evolution of disparate collective behaviours in other animal groups and among cells within developing animals. Together, these studies illuminate the life history of O. biroi, and suggest mechanisms for the evolution of core aspects of cooperative behaviour in ant colonies. I draw comparisons to the evolution of superorganismality in other lineages, as well as to the evolution of multicellularity. I suggest that there may be additional similarities in the proximate evolutionary trajectories of superorganismality and multicellularity. ACKNOWLEDGEMENTS The work in this dissertation was only possible because of the collaboration, advice, and encouragement of a large number of people. First, and most importantly, I wish to thank my advisor, Daniel Kronauer. For all of Daniel’s generosity, encouragement, patience, and wisdom; for giving me the freedom to explore my ideas; for guiding me to better questions and to satisfying answers with kindness and foresight; and for introducing me to the wonder of ant societies, I am immensely grateful. I am very grateful to Leonora Olivos-Cisneros and Stephany Valdes Rodriguez for all that they do to keep the lab going, for rearing many of the ants I needed for my experiments, for teaching me (repeatedly) how to keep them alive, and for much else. Over the course of my PhD, I have collaborated considerably with many members of the Kronauer lab. The work in Chapter 2 was done in collaboration with Ingrid Fetter- Pruneda, and we shared lead authorship of a published article about this work (Chandra et al., 2018). Ingrid taught me immunohistochemistry, and spearheaded the development of insulin antibodies, synthetic peptides, ovary and immunostaining assays, and more. Several other lab members also made essential contributions to this work. I use the pronoun “we” extensively in Chapter 2 (and in the associated sections of Chapters 5 and 6) to acknowledge the collaborative nature of this project. Peter Oxley initiated this project, designed (and conducted much of) the transcriptomic screen, and introduced me – with tolerance and generosity - to comparative genomics. Amelia Ritger helped with peptide injections, immunohistochemistry, ant painting, and much else. Yuko Ulrich introduced me to the behaviour of clonal raider ants, and to the study of their division of labour. Much of the work in Chapter 4 was done in collaboration with Asaf Gal, who iii taught me much about automated tracking and behavioural analysis, and who made crucial contributions to the design and interpretation of this project. Sean McKenzie helped me in more ways than I can name; as a collaborator (from whom I learnt much) on the genomic analyses in Chapter 2, as an unreasonably indulgent benchmate always willing to engage thoughtfully with my half-baked ideas, and as a co- conspirator in the pursuit of greater caffeination. Similarly, Buck Trible improved my work in innumerable ways, painstakingly helping me refine my thinking, and by always being willing to talk about ants and evolution. Many other members of the Kronauer lab, past and present, have also contributed intellectually to my work - including Taylor Hart, Iryna Ivasyk, Kip Lacy, Romain Libbrecht, Dennis Melendez, Patrick Piekarski, and Karen Sun. It has been a delight to be part of the Clonal Raider Ant Project with you all. I received a great deal of support elsewhere at the Rockefeller too. I am very grateful to the members of my Thesis Committee, Leslie Vosshall, Cori Bargmann, and Gaby Maimon for their invaluable advice and encouragement, and for teaching me to be both more realistic and more ambitious. Thanks as well to Hopi Hoekstra, my external examiner, for taking the time to examine this thesis. To all these people, and to the many others who have also been generous with their time and their wisdom, I am deeply indebted. Thanks also to the Rockefeller University Resource Centers, and to their members: especially Jim Petrillo, Connie Zhao, Tao Tong, and Lavoisier Ramos-Espiritu for technical advice and assistance. And thanks to the BSVMRKYZ meetings, the Evolution Journal Club, and the Faculty and Students’ Club for intellectual stimulation and libations. Thanks to Mark Deyrup and the Archbold Biological Station for their hospitality and assistance with ant collection. I am also grateful to the scientific societies I have been iv part of, and whose meetings I have been fortunate to attend: especially the International Union for the Study of Social Insects (North American Section), Social INsects in the North East RegionS [sic], the Jürgen Wheeler Social Society for Statistical Myrmecology, and the Pan-American Society for Evolutionary Developmental Biology. The conversations I have had with colleagues through these societies have greatly enriched my work. I am especially grateful to Simon Garnier, Mary Jane West-Eberhard, Adria LeBoeuf, and Lior Baltiansky, who have all improved my understanding of various aspects of sociobiology. Thanks also to Emily Atlas, Adele Bubnys, Eduardo Dias Ferreira, Taylor Hart, Iryna Ivasyk, Sean McKenzie, Hilary Monaco, Alex Paul, Buck Trible, Vikram Vijayan, and Jazz Weisman for friendship, conversation, and much else. To them, and to everybody else who enlivened my time at the Rockefeller, I am grateful. Finally, I am enormously grateful to my family, for teaching me to be curious, and for their unwavering love, support, and interest in my nutritional state. Thanks especially to my cousin Sharan Prakash, who induced my differentiation into a biologist and has since maintained my sanity homeostatically, to my sister Aditi Chandra, for her enthusiasm, solidarity, and vague helpfulness, and to my parents, Nagasuma and Satish Chandra, to whom I owe everything. None of this would be possible without them. v TABLE OF CONTENTS MECHANISMS FOR THE EVOLUTION OF SUPERORGANISMALITY IN ANTS I ACKNOWLEDGEMENTS
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