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The evolution of eusociality in Hymenoptera—encompassing bees, ants, and wasps—is characterized by multiple gains and losses of social living, making this group a prime model to understand the mechanisms that underlie social behavior and social complexity. Our review synthesizes insights into the evolutionary history and molecular basis of eusociality. We examine new evidence for key evolutionary hypotheses and molecular pathways that regulate social behaviors, highlighting convergent evolution on a shared molecular toolkit that includes the insulin/insulin-like growth factor signaling (IIS) and target of rapamycin (TOR) pathways, juvenile hormone and ecdysteroid signaling, and epigenetic regulation. We emphasize how the crosstalk among these nutrient-sensing and endocrine signaling pathways enables social insects to integrate external environmental stimuli, including social cues, with internal physiology and behavior. We argue that examining these pathways as an integrated regulatory circuit and exploring how the regulatory architecture of this circuit evolves alongside eusociality can open the door to understanding the origin of the complex life histories and behaviors of this group.
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Co-expression Gene Networks and Machine-learning Algorithms Unveil a Core Genetic Toolkit for Reproductive Division of Labour in Rudimentary Insect Societies
Abstract The evolution of eusociality requires that individuals forgo some or all their own reproduction to assist the reproduction of others in their group, such as a primary egg-laying queen. A major open question is how genes and genetic pathways sculpt the evolution of eusociality, especially in rudimentary forms of sociality—those with smaller cooperative nests when compared with species such as honeybees that possess large societies. We lack comprehensive comparative studies examining shared patterns and processes across multiple social lineages. Here we examine the mechanisms of molecular convergence across two lineages of bees and wasps exhibiting such rudimentary societies. These societies consist of few individuals and their life histories range from facultative to obligately social. Using six species across four independent origins of sociality, we conduct a comparative meta-analysis of publicly available transcriptomes. Standard methods detected little similarity in patterns of differential gene expression in brain transcriptomes among reproductive and non-reproductive individuals across species. By contrast, both supervised machine learning and consensus co-expression network approaches uncovered sets of genes with conserved expression patterns among reproductive and non-reproductive phenotypes across species. These sets overlap substantially, and may comprise a shared genetic “toolkit” for sociality across the distantly related taxa of bees and wasps and independently evolved lineages of sociality. We also found many lineage-specific genes and co-expression modules associated with social phenotypes and possible signatures of shared life-history traits. These results reveal how taxon-specific molecular mechanisms complement a core toolkit of molecular processes in sculpting traits related to the evolution of eusociality.
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- Award ID(s):
- 1929239
- PAR ID:
- 10469660
- Editor(s):
- Webster, Matthew
- Publisher / Repository:
- Oxford
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/gbe/evac174
