Factors and mechanisms of queen behavioral flexibility in the ants
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Abstract
A key aspect of eusocial societies is the division of labor, where individuals specialize in reproductive and non-reproductive tasks. Within eusocial insect colonies, non-reproductive workers perform essential tasks, such as foraging, nest maintenance, defense, and brood care, while reproductive queens focus primarily on egg-laying.
Ants, in particular, exhibit extraordinary diversity in their social systems. The ant queen has been traditionally seen as a specialized reproductive unit, yet during colony foundation, queens can perform diverse behaviors including brood care. Its behavior becomes increasingly specialized as workers emerge. However, recent research has shown that this specialization is reversible and queens can express several non-reproductive behaviors upon changes in the social environment. Despite this, we still lack a fundamental understanding of how queen behavior is shaped across the ant phylogeny, and how social context and underlying molecular processes modulate behavioral flexibility.
To address these questions, I employed three complementary approaches. First, I conducted a broad phylogenetic investigation of queen behavioral flexibility across 38 ant species, using standardized behavioral assays. This analysis revealed that behavioral plasticity in queens is widespread, though it varies greatly across lineages. The social structure of species explained some of the variation. Second, I focused on intraspecific variation of queens in polygynous queens of the Amblyoponinae Stigmatomma pallipes showing that queens differ in mobility and mating status. Crucially, by generating a high-quality reference genome and comparing tissue-specific transcriptomes, I reveal that unmated queens express gene expression profiles closely resembling those of workers. Therefore, elucidating that the molecular underpinnings of behavior are not bound by morphology alone. Third, I investigated the molecular mechanisms regulating queen behavioral reversibility in the ant Lasius niger. Using gene expression profiling, I identified 123 genes that differed in the brains of queens depending on the presence or absence of workers. Among these, I identified a subset of genes that are known to modulate behavioral plasticity in insects, such as Krüppel-homolog 1 (Kr-h1), and parts of the insulin-like signaling pathway.
Together, this thesis demonstrates that queen behavioral flexibility is a widely conserved yet not fixed trait in ants, which is shaped by both social context and molecular regulation. These insights deepen our understanding of how specialized roles, whether in insect societies or other complex systems, are maintained and modulated. Ultimately, this work contributes to a broader framework for understanding how division of labor emerges and is maintained in biological systems, emphasizing the importance of variation within a highly specialized role.