Student Theses and Dissertations

Date of Award

2021

Document Type

Thesis

Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Kronauer Laboratory

Abstract

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.

Comments

A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy

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