The evolution and mechanisms of caste plasticity in vespid wasps

Social insects are ecologically dominant predators, pollinators, herbivores and detritivores across many terrestrial ecosystems. Key to the ecological success of these species is a uniquely strong division of labour between reproductives (‘queens’) and non-reproductives (‘workers’). In some social insect species, reproductive division of labour is obligate and developmentally determined, but many other taxa possess full reproductive plasticity, which is the basal state for social insect evolution. Answering the question of how division of reproductive labour is maintained in the presence of reproductive plasticity is an important prerequisite to understanding how and why this plasticity has been lost in the most derived social insect taxa. In this thesis, I address this question using two species of social wasp which exhibit strong division of reproductive labour but full reproductive plasticity. Two chapters of the thesis examine responses to queen loss in the European paper wasp P. dominula, in order to understand the mechanisms by which groups accommodate the loss of a reproductive. In Chapter 2 I show that in this species, groups generate replacement reproductives rapidly and with little conflict by relying on an age-based succession criterion. In Chapter 3 I analyse the transcriptomic mechanisms that underlie this succession process, and show that variation in individuals’ phenotypes only partially explains their transcriptomic responses, a result that suggests hidden costs of queen loss. In Chapter 4, I analyse individual-level transcriptomic data from a facultatively social tropical hover wasp, Liostenogaster flavolineata, which forms linearly age-based dominance hierarchies in which individuals exhibit progressively reduced foraging effort as they move up in rank. I show that despite differences in social structure, variation in gene expression in colonies of this species is surprisingly similar to that of obligately social species such as P. dominula. I also find that genes that are associated with indirect fitness in L. flavolineata are more strongly evolutionarily conserved than genes associated with direct fitness, a surprising result that runs counter to results obtained for other social insect species. Additionally, in Chapter 5 I argue for a reconceptualization of the loss of reproductive plasticity that has occurred in more complex insect societies. Taken as a whole, this thesis sheds light on the behavioural and transcriptomic mechanisms by which distinct fitness strategies are maintained in reproductively skewed societies as well as revealing potential limitations of these mechanisms, emphasising the value of reproductively plastic social insects as models for the evolution of sociality

IST Austria Thesis

Social insect colonies tend to have numerous members which function together like a single organism in such harmony that the term ``super-organism'' is often used. In this analogy the reproductive caste is analogous to the primordial germ cells of a metazoan, while the sterile worker caste corresponds to somatic cells. The worker castes, like tissues, are in charge of all functions of a living being, besides reproduction. The establishment of new super-organismal units (i.e. new colonies) is accomplished by the co-dependent castes. The term oftentimes goes beyond a metaphor. We invoke it when we speak about the metabolic rate, thermoregulation, nutrient regulation and gas exchange of a social insect colony. Furthermore, we assert that the super-organism has an immune system, and benefits from ``social immunity''. Social immunity was first summoned by evolutionary biologists to resolve the apparent discrepancy between the expected high frequency of disease outbreak amongst numerous, closely related tightly-interacting hosts, living in stable and microbially-rich environments, against the exceptionally scarce epidemic accounts in natural populations. Social immunity comprises a multi-layer assembly of behaviours which have evolved to effectively keep the pathogenic enemies of a colony at bay. The field of social immunity has drawn interest, as it becomes increasingly urgent to stop the collapse of pollinator species and curb the growth of invasive pests. In the past decade, several mechanisms of social immune responses have been dissected, but many more questions remain open. I present my work in two experimental chapters. In the first, I use invasive garden ants (*Lasius neglectus*) to study how pathogen load and its distribution among nestmates affect the grooming response of the group. Any given group of ants will carry out the same total grooming work, but will direct their grooming effort towards individuals carrying a relatively higher spore load. Contrary to expectation, the highest risk of transmission does not stem from grooming highly contaminated ants, but instead, we suggest that the grooming response likely minimizes spore loss to the environment, reducing contamination from inadvertent pickup from the substrate. The second is a comparative developmental approach. I follow black garden ant queens (*Lasius niger*) and their colonies from mating flight, through hibernation for a year. Colonies which grow fast from the start, have a lower chance of survival through hibernation, and those which survive grow at a lower pace later. This is true for colonies of naive and challenged queens. Early pathogen exposure of the queens changes colony dynamics in an unexpected way: colonies from exposed queens are more likely to grow slowly and recover in numbers only after they survive hibernation. In addition to the two experimental chapters, this thesis includes a co-authored published review on organisational immunity, where we enlist the experimental evidence and theoretical framework on which this hypothesis is built, identify the caveats and underline how the field is ripe to overcome them. In a final chapter, I describe my part in two collaborative efforts, one to develop an image-based tracker, and the second to develop a classifier for ant behaviour

Individuality and consistency in foraging behaviour of the Bumblebee Bombus terrestris

PhDMany vertebrates and a few invertebrates are known to show individual-specific consistency in their behaviour across time and situations, sometimes in ways that can be paralleled with human personality. Despite their relatively small brains, bees show remarkable cognitive abilities. It is therefore not unreasonable to speculate that, as other animals with such cognitive abilities, they too would be able to show some form of animal personality. The first three chapters of this work are theoretical and discuss relevant concepts and controversies in the field of animal personality. Chapter 4 explored the possibility of individual bees differing in their ability to learn to associate stimuli with reward. While some bees learned to differentiate between two stimuli with a high degree of accuracy, others made frequent mistakes, independently of the modality or dimension of the stimuli considered. Bees therefore appeared to differ individually in their ability to discriminate between stimuli. Chapter 5 of this work aimed at answering the question of whether individual bees consistently differ in their behaviour, which is a prerequisite to establishing the existence of personality in any animal. Individual bees’ response to novelty (neophobianeophilia) was found to be relatively predictable within a short time scale but not on the long term. Neophobia-neophilia is therefore an episodic personality trait. Chapter 6 was concerned with individual responses to a simulated predation threat. Individual bees were found to vary widely, both qualitatively and quantitatively. These responses were consistent through time and so were other features of their foraging behaviours. Taken together, my findings provide an insight into individual variations in foraging behaviour in the bumblebee Bombus terrestris and represent good evidence for the existence of individual consistency, thus paving the way for further research into personality traits in this species

Mechanisms for the Evolution of Superorganismality in Ants

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

Emergent Behavior Development and Control in Multi-Agent Systems

Emergence in natural systems is the development of complex behaviors that result from the aggregation of simple agent-to-agent and agent-to-environment interactions. Emergence research intersects with many disciplines such as physics, biology, and ecology and provides a theoretical framework for investigating how order appears to spontaneously arise in complex adaptive systems. In biological systems, emergent behaviors allow simple agents to collectively accomplish multiple tasks in highly dynamic environments; ensuring system survival. These systems all display similar properties: self-organized hierarchies, robustness, adaptability, and decentralized task execution. However, current algorithmic approaches merely present theoretical models without showing how these models actually create hierarchical, emergent systems. To fill this research gap, this dissertation presents an algorithm based on entropy and speciation - defined as morphological or physiological differences in a population - that results in hierarchical emergent phenomena in multi-agent systems. Results show that speciation creates system hierarchies composed of goal-aligned entities, i.e. niches. As niche actions aggregate into more complex behaviors, more levels emerge within the system hierarchy, eventually resulting in a system that can meet multiple tasks and is robust to environmental changes. Speciation provides a powerful tool for creating goal-aligned, decentralized systems that are inherently robust and adaptable, meeting the scalability demands of current, multi-agent system design. Results in base defense, k-n assignment, division of labor and resource competition experiments, show that speciated populations create hierarchical self-organized systems, meet multiple tasks and are more robust to environmental change than non-speciated populations

Evolving Specialization in an Agent-Based Model without Task-Switching Costs

This work examines the possibility of evolving the phenotypic specialization associated with division of labor in an agent-based model without task-switching costs. The model examines two groups competing for vital resources, where members of one group are capable of sharing resources with other agents in their group. Agents attempt to collect resources which allow them to reproduce, with more resources leading to a greater number of offspring by asexual reproduction. Four variants of the model are examined, with combinations of one or two resources and the presence of a foraging risk. The presence of the foraging risk can lead to agents in the sharing group specializing in each trait but, by looking at the fraction of foragers per generation, this event appears to be a transient state. Division of labor is quantified by calculating the normalized mutual entropy, and is shown to be higher when a population contains agents which specialize on different tasks

Evolving specialization in an agent-based model without task-switching costs

This work examines the possibility of evolving the phenotypic specialization associated with division of labor in an agent-based model without task-switching costs. The model examines two groups competing for vital resources, where members of one group are capable of sharing resources with other agents in their group. Agents attempt to collect resources which allow them to reproduce, with more resources leading to a greater number of offspring by asexual reproduction. Four variants of the model are examined, with combinations of one or two resources and the presence of a foraging risk. The presence of the foraging risk can lead to agents in the sharing group specializing in each trait but, by looking at the fraction of foragers per generation, this event appears to be a transient state. Division of labor is quantified by calculating the normalized mutual entropy, and is shown to be higher when a population contains agents which specialize on different tasks --Abstract, page iii

Social Algorithms

This article concerns the review of a special class of swarm intelligence based algorithms for solving optimization problems and these algorithms can be referred to as social algorithms. Social algorithms use multiple agents and the social interactions to design rules for algorithms so as to mimic certain successful characteristics of the social/biological systems such as ants, bees, bats, birds and animals.Comment: Encyclopedia of Complexity and Systems Science, 201