Abstract
Comparative genomic 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 self-transcribing active regulatory region sequencing, 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 3 social and 3 solitary populations. Many enhancers were identified in only a subset of L. albipes populations, revealing rapid divergence in regulatory regions within this species. 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 1,182 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 associated with the fine-tuning of ancient enhancers as well as lineage-specific regulatory changes. Combining enhancer activity with population genetic data revealed 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.
Document Type
Article
Publication Date
11-2024
Digital Object Identifier (DOI)
https://doi.org/10.1093/molbev/msae229
Funding Information
This work was supported by grant no. DEB 1754476 from the National Science Foundation, and S.D.K. was supported by the National Institutes of Health New Innovator Award (1DP2GM137424-01), the Packard Foundation, and the Pew Biomedical Scholars program. S.D.K. is an HHMI Freeman Hrabowski Scholar. Lasioglossum albipes was se- quenced as part of the I5K and USDA-ARS Beenome100 ini- tiative. The US Department of Agriculture, Agricultural Research Service is an equal opportunity/affirmative action employer, and all agency services are available without dis- crimination. This research used resources provided by the SCINet project of the USDA Agricultural Research Service, ARS project number 0500-00093-001-00-D, the Tropical Pest Genetics and Molecular Biology Research Unit in-house appropriated research project number 2040-22430-028-000-D, and the Genetics and Bioinformatics Research Unit in-house appropriated re- search project number 6066-21310-006-000-D.
Repository Citation
Jones, Beryl M.; Webb, Andrew E.; Geib, Scott M.; Sim, Sheina; Schweizer, Rena M.; Branstetter, Michael G.; Evans, Jay D.; and Kocher, Sarah D., "Repeated Shifts in Sociality Are Associated With Fine-tuning of Highly Conserved and Lineage-Specific Enhancers in a Socially Flexible Bee" (2024). Entomology Faculty Publications. 254.
https://uknowledge.uky.edu/entomology_facpub/254
Included in
Ecology and Evolutionary Biology Commons, Entomology Commons, Genetics Commons, Molecular Biology Commons
Notes/Citation Information
© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.