Time-course RNASeq ofCamponotus floridanusforager and nurse ant brains indicate links between plasticity in the biological clock and behavioral division of labor

Abstract

AbstractBackgroundCircadian clocks allow organisms to anticipate daily fluctuations in their environment by driving rhythms in physiology and behavior. Inter-organismal differences in daily rhythms, called chronotypes, exist and can shift with age. In ants, age, caste-related behavior and chronotype appear to be linked. “Around-the-clock” active nurse ants are usually younger and, with age, transition into rhythmically active foragers. Moreover, ants can shift between these behavioral castes depending on social context. We investigated how changes in daily gene expression could be contributing to such behavioral plasticity inCamponotus floridanuscarpenter ants by combining time-course behavioral assays and RNA-Sequencing of forager and nurse brains.ResultsWe found that nurse brains have three times fewer 24h oscillating genes than foragers. However, several hundred genes that oscillated every 24h in forager brains showed robust 8h oscillations in nurses, including the core clock genesPeriodandShaggy. These differentially rhythmic genes consisted of several components of the circadian entrainment pathway, and showed enrichments for functions related to metabolism, cellular communication and protein modification. We additionally found thatVitellogenin, known to regulate division of labor in social insects, showed robust 24h oscillations in nurse brains but not in foragers. Furthermore, the protein products of several genes that were differentially expressed between the two ant castes were previously found in the trophallactic fluid ofC. floridanus. This suggests a putative role for trophallaxis in regulating behavioral division of labor through caste-specific gene expression.ConclusionWe provide a first look at the chronobiological differences in gene expression between forager and nurse ant brains. This endeavor allowed us to identify putative molecular mechanisms underlying plastic timekeeping. Several components of the ant circadian clock and its output can seemingly oscillate at different harmonics of the circadian rhythm. We propose that such chronobiological plasticity has evolved to allow for distinct regulatory networks that underlie behavioral castes, while supporting swift caste transitions in response to colony demands. Behavioral division of labor is common among social insects. The links between chronobiological and behavioral plasticity that we found inC. floridanus, thus, likely represent a more general phenomenon that warrants further investigation.