Neurogenomic architecture of honey bee social behavior

Animals adaptively navigate complex social interactions, respond to social signals, and modify behavior to meet the demands of a changing environment. To do so, social experience must be embedded in the nervous system to modify behavior in anticipation of future events. How social information is encoded in the brain and informs social decision-making, and how this process is shaped by the environment, are fundamental questions in neuroscience. In this dissertation, I address these questions by deploying systems-level approaches to understanding layers of neurogenomic and social organization in the western honey bee (Apis mellifera). This dissertation consists of original research on the neurogenomic architecture of social behavior in honey bees. Honey bees form highly complex societies and exhibit rich behavioral repertoires generated by a tiny brain of ~1,000,000 neurons. I leverage naturally occurring honey bee behavior to elucidate molecular mechanisms that process environmental information and give rise to social organization. In Chapter 1, I review current literature regarding the neurogenomic basis of social interactions, with emphasis on progress in honey bee research. This Chapter also introduces major themes addressed by my dissertation research, including social decision-making and biological embedding, and was prepared as an invited review article for Annual Review of Neuroscience. In Chapter 2, I identify regions of the honey bee brain that are differentially activated across affiliative and agonistic social contexts, elucidating neuronal organizational strategies for encoding complex social information in a tiny brain. This Chapter is published in Proceedings of the Royal Society B: Biological Sciences. In Chapter 3, I explore how adverse social experience influences future decision-making. I show that acute exposure to threat modifies individual and group behavior, and that these changes are associated with experience-dependent patterns of brain gene expression. In Chapter 4, I leverage a combination of published and new transcriptomic datasets to perform a meta-analysis of honey bee neurogenomic response to infection with a common virus, Deformed wing, that impacts behavior, health, and survival. This Chapter is published in Scientific Reports. Finally, in Chapter 5, I describe how honey bee colony aggression, an emergent group behavioral trait, is related to variation in the neurogenomic architecture of individual honey bee workers. This analysis utilizes brain transcriptomics to implicate molecular programs, brain cell types, and gene regulatory networks that contribute to individual-level differences in behavioral state, and I go on to describe how this molecular variation is in turn shaped by colony environment. Taken together, this dissertation contributes to our understanding of how brain, genome and behavior interact in honey bees, with potential applications for all social animals.

Name thesis:degree_name

Ph.D.

Level thesis:degree_level

Dissertation

Discipline thesis:degree_discipline

Neuroscience

Grantor

University of Illinois at Urbana-Champaign

Year dc:date

2021

Author dc:creator

• Traniello, Ian Michael

Contributors dc:contributor

• Robinson, Gene E
• Gillette, Martha
• Bell, Alison
• Grosman, Claudio

• neurogenomics
• social decision-making
• biological embedding
• valence

Statement dc:rights

• Copyright 2020 Ian M. Traniello

Language dc:language

en

Handle dc:identifier

http://hdl.handle.net/2142/109580

OAI identifier oai:identifier

oai:www.ideals.illinois.edu:2142/109580