Individual differences in honey bee behavior enabled by plasticity in brain gene regulatory networks

Beryl M. Jones; Vikyath D. Rao; Tim Gernat; Tobias Jagla; Amy C. Cash-Ahmed; Benjamin E.R. Rubin; Troy J. Comi; Shounak Bhogale; Syed S. Husain; Charles Blatti; Martin Middendorf; Saurabh Sinha; Sriram Chandrasekaran; Gene E. Robinson

doi:10.7554/eLife.62850

Individual differences in honey bee behavior enabled by plasticity in brain gene regulatory networks

Beryl M. Jones, Vikyath D. Rao, Tim Gernat, Tobias Jagla, Amy C. Cash-Ahmed, Benjamin E.R. Rubin, Troy J. Comi, Shounak Bhogale, Syed S. Husain, Charles Blatti, Martin Middendorf, Saurabh Sinha, Sriram Chandrasekaran, Gene E. Robinson

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

Understanding the regulatory architecture of phenotypic variation is a fundamental goal in biology, but connections between gene regulatory network (GRN) activity and individual differences in behavior are poorly understood. We characterized the molecular basis of behavioral plasticity in queenless honey bee (Apis mellifera) colonies, where individuals engage in both reproductive and non-reproductive behaviors. Using high-throughput behavioral tracking, we discovered these colonies contain a continuum of phenotypes, with some individuals specialized for either egg-laying or foraging and ‘generalists’ that perform both. Brain gene expression and chromatin accessibility profiles were correlated with behavioral variation, with generalists intermediate in behavior and molecular profiles. Models of brain GRNs constructed for individuals revealed that transcription factor (TF) activity was highly predictive of behavior, and behavior- associated regulatory regions had more TF motifs. These results provide new insights into the important role played by brain GRN plasticity in the regulation of behavior, with implications for social evolution.

Original language	English
Article number	e62850
Pages (from-to)	1-28
Number of pages	28
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.62850
State	Published - Dec 2020

Bibliographical note

Publisher Copyright:
© Jones et al.

Funding

We thank A Sankey, A Ray, S Bransley, J Cullum, K Wilk and J Falk for assistance in the field, A Her-nandez and the staff at the Carver Biotechnology Center for sequencing services, administrators of Biocluster (UIUC) for computational support, and MB Sokolowski, M Hudson, AM Bell, members of the Robinson lab, and three anonymous reviewers for comments that improved this manuscript. Funding: This research was supported by Grant R01GM117467 from the National Institute of General Medical Sciences (GER and N Goldenfeld, PIs), the Christopher Foundation (GER), and the Illinois Sociogenomics Initiative (GER). Data and materials availability: The raw sequence data reported in this paper have been deposited at the National Center for Biotechnology Information (NCBI) Sequence Read Archive, Accession PRJNA593999. Requests for materials should be addressed to BMJ. This research was supported by Grant R01GM117467 from the National Institute of Gen-eral Medical Sciences (GER and N Goldenfeld, PIs), the Christopher Foundation (GER), and the Illi-nois Sociogenomics Initiative (GER).

Funders	Funder number
Christopher Family Foundation
Ger. Psychiat. Assoc., Ev. A.
Illi-nois Sociogenomics Initiative
Illinois Sociogenomics Initiative
National Institute of General Medical Sciences	R01GM117467
National Institute of General Medical Sciences
Christopher and Dana Reeve Foundation

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
General Immunology and Microbiology

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Jones, B. M., Rao, V. D., Gernat, T., Jagla, T., Cash-Ahmed, A. C., Rubin, B. E. R., Comi, T. J., Bhogale, S., Husain, S. S., Blatti, C., Middendorf, M., Sinha, S., Chandrasekaran, S., & Robinson, G. E. (2020). Individual differences in honey bee behavior enabled by plasticity in brain gene regulatory networks. eLife, 9, 1-28. Article e62850. https://doi.org/10.7554/eLife.62850

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abstract = "Understanding the regulatory architecture of phenotypic variation is a fundamental goal in biology, but connections between gene regulatory network (GRN) activity and individual differences in behavior are poorly understood. We characterized the molecular basis of behavioral plasticity in queenless honey bee (Apis mellifera) colonies, where individuals engage in both reproductive and non-reproductive behaviors. Using high-throughput behavioral tracking, we discovered these colonies contain a continuum of phenotypes, with some individuals specialized for either egg-laying or foraging and {\textquoteleft}generalists{\textquoteright} that perform both. Brain gene expression and chromatin accessibility profiles were correlated with behavioral variation, with generalists intermediate in behavior and molecular profiles. Models of brain GRNs constructed for individuals revealed that transcription factor (TF) activity was highly predictive of behavior, and behavior- associated regulatory regions had more TF motifs. These results provide new insights into the important role played by brain GRN plasticity in the regulation of behavior, with implications for social evolution.",

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Individual differences in honey bee behavior enabled by plasticity in brain gene regulatory networks

Abstract

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ASJC Scopus subject areas

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