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ARS Home » Pacific West Area » Hilo, Hawaii » Daniel K. Inouye U.S. Pacific Basin Agricultural Research Center » Tropical Pest Genetics and Molecular Biology Research Unit » Research » Publications at this Location » Publication #418098

Research Project: Advancing Molecular Pest Management, Diagnostics, and Eradication of Fruit Flies and Invasive Species

Location: Tropical Pest Genetics and Molecular Biology Research Unit

Title: Repeated shifts in sociality are associated with fine-tuning of highly conserved and lineage-specific enhancers in a socially flexible bee

Author
item JONES, BERYL - University Of Kentucky
item WEBB, ANDREW - Princeton University
item Geib, Scott
item Sim, Sheina
item Schweizer, Rena
item Branstetter, Michael
item Evans, Jay
item KOCHER, SARAH - Princeton University

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 8/21/2024
Publication Date: 8/21/2024
Citation: Jones, B.M., Webb, A.E., Geib, S.M., Sim, S.B., Schweizer, R.M., Branstetter, M.G., Evans, J.D., Kocher, S.D. 2024. Repeated shifts in sociality are associated with fine-tuning of highly conserved and lineage-specific enhancers in a socially flexible bee. bioRxiv. https://doi.org/10.1101/2024.08.15.608154.
DOI: https://doi.org/10.1101/2024.08.15.608154

Interpretive Summary: Lasioglossum albipes is a sweat bee species that exists in both solitary and social forms. Here we present a chromosome scale genome assembly and annotation of this species and apply a sequining technique to characterize the architecture of transcriptional enhancers, between social and solitary individuals of this species. Enhancers are components of the genome that can modify the expression of specific genes over time and localization within a organism. It is thought that changes in these regulatory controllers can explain some of the physiological and behavioral differences between soliary and social individuals in this species. By comparing the profiles of enhancer sequences identified in this study, 1182 putative enhancers shows significant difference between the social and solitary populations. This study provides foundational evidence of how regulatory regions across the genome can be playing a role in sociality within this species, and potentially across bees more generally.

Technical Abstract: Comparative genomics studies of social insects suggest that changes in gene regulation are associated with evolutionary transitions in social behavior, but the activity of predicted regulatory regions has not been tested empirically. We used STARR-seq, a high-throughput enhancer discovery tool, to identify and measure the activity of enhancers in the socially variable sweat bee, Lasioglossum albipes. We identified over 36,000 enhancers in the L. albipes genome from three social and three solitary populations. Many enhancers were identified in only a subset of populations, revealing rapid divergence in regulatory regions of L. albipes. Population-specific enhancers were often proximal to the same genes across populations, suggesting compensatory gains and losses of regulatory regions may preserve gene activity. We also identified 1182 enhancers with significant differences in activity between social and solitary populations, some of which are conserved regulatory regions across species of bees. These results indicate that social trait variation in L. albipes is driven both by the fine-tuning of ancient enhancers as well as lineage-specific regulatory changes. Combining enhancer activity with population genetics data of the same populations revealed genetic variants associated with differences in enhancer activity and identified a subset of differential enhancers with signatures of selection associated with social behavior. Together, these results provide the first empirical map of enhancers in a socially flexible bee and highlight links between cis-regulatory variation and the evolution of social behavior.