Abstract
A key question in the rising field of neuroepigenetics is how behavioral plasticity is established and maintained in the developing CNS of multicellular organisms. Behavior is controlled through systemic changes in hormonal signaling, cell-specific regulation of gene expression, and changes in neuronal connections in the nervous system, however the link between these pathways is unclear. In the ant Camponotus floridanus, the epigenetic corepressor CoREST is a central player in experimentally-induced reprogramming of caste-specific behavior, from soldier (Major worker) to forager (Minor worker). Here, we show this pathway is engaged naturally on a large genomic scale during late pupal development targeting multiple genes differentially expressed between castes, and central to this mechanism is the protein tramtrack (ttk), a DNA binding partner of CoREST. Caste-specific differences in DNA binding of ttk co-binding with CoREST correlate with caste-biased gene expression both in the late pupal stage and immediately after eclosion. However, we find a unique set of exclusive Minor-bound genes that show ttk pre-binding in the late pupal stage preceding CoREST binding, followed by caste-specific gene repression on the first day of eclosion. In addition, we show that ttk binding correlates with neurogenic Notch signaling, and that specific ttk binding between castes is enriched for regulatory sites associated with hormonal function. Overall our findings elucidate a pathway of transcription factor binding leading to a repressive epigenetic axis that lies at the crux of development and hormonal signaling to define worker caste identity in C. floridanus.
Highlights
Based upon environmental cues, members of a eusocial insect colony have the ability to differentiate into morphologically and behaviorally-distinct sterile or reproductive physiological castes [1]
We find that in the Florida Carpenter Ant C. floridanus two members of a known repressive complex, CoREST and ttk, are predictive of early-life gene expression differences between Major and Minor workers, which display vastly different behaviors
In conjunction with the large number of gene expression differences seen at d0 which are greatly reduced by d5 [2], we hypothesized that the late pupal stage (LPS)-d0 ages represent a crucial time for behavioral specification in natural caste development, and that CoREST may act definitively at this stage compared to later adult timepoints
Summary
Members of a eusocial insect colony have the ability to differentiate into morphologically and behaviorally-distinct sterile (worker) or reproductive (queen) physiological castes [1]. Despite sharing genotypes, members of a colony exhibit dramatic phenotypic and behavioral distinctions more akin to differences between species. Because of this extreme phenotypic and behavioral plasticity in the context of highly related individuals, eusocial insects have emerged as models for interrogating complex social behavior, and for investigating molecular mechanisms that program this remarkable plasticity [6, 7]. Central to the establishment of differential chromatin modification are transcription factors (TFs) that recruit co-factors that in turn modify chromatin or provide a scaffold for assembly of modifiers; these gene regulatory assemblies serve as gene-proximal signal integrators that activate transcription and lead to longer-lasting changes in underlying chromatin for cell type specification [16, 17]
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