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We examined the overlap in the genes associated with daily rhythms and with behavioral plasticity in ants. We first investigated the daily rhythms of gene expression in the harvester ant,Pogonomyrmex barbatus, and how the rhythmic genes overlap with others previously shown to be associated with plasticity of foraging behavior. Then, to consider whether the overlap is conserved across ant species, we compared rhythms of gene expression in the diurnal, desert harvester ants with those previously reported for a distantly related nocturnal, subtropical carpenter ant,Camponotus floridanus. First, daily transcriptomes inP. barbatusshowed that most genes were expressed in light-dark (LD) and constantly dark (DD) conditions at about the same levels; only 11 genes showed at least a two-fold change in expression. Network analysis identified eleven modules ofP. barbatusgenes under LD conditions. Of these 11 clusters, modules C1 and C2 seem to be central nodes of the gene expression network, because they are the most highly connected in LD, and show the strongest preservation in DD vs. LD, and contain core clock genePeriod. Only one module, C2, showed significant overlap withP. barbatusgenes that have 24h-rhythmic expression in both LD and DD. There was significant overlap between modules C1, C2, C10, C11, andP. barbatusgenes found previously to be associated with plasticity in the regulation of foraging activity to manage water loss. A comparison of the daily transcriptome ofP. barbatuswith that ofC. floridanusshowed significant overlap of 24h-rhythmic genes in LD. Modules C1 and C2 of P. barbatus also overlap withC. floridanusgenes previously shown to differ in expression rhythms in nurses and foragers. In combination, these results indicate that genes linking plasticity of the circadian clock and of behavior may be broadly conserved in ants.
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Time-course RNASeq of Camponotus floridanus forager and nurse ant brains indicate links between plasticity in the biological clock and behavioral division of labor
Abstract Background Circadian 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. Brood-tending nurse ants are usually younger individuals and show “around-the-clock” activity. With age or in the absence of brood, nurses transition into foraging ants that show daily rhythms in activity. Ants can adaptively shift between these behavioral castes and caste-associated chronotypes depending on social context. We investigated how changes in daily gene expression could be contributing to such behavioral plasticity in Camponotus floridanus carpenter ants by combining time-course behavioral assays and RNA-Sequencing of forager and nurse brains. Results We found that nurse brains have three times fewer 24 h oscillating genes than foragers. However, several hundred genes that oscillated every 24 h in forager brains showed robust 8 h oscillations in nurses, including the core clock genes Period and Shaggy . These differentially rhythmic genes consisted of several components of the circadian entrainment and output pathway, including genes said to be involved in regulating insect locomotory behavior. We also found that Vitellogenin , known to regulate division of labor in social insects, showed robust 24 h oscillations in nurse brains but not in foragers. Finally, we found significant overlap between genes differentially expressed between the two ant castes and genes that show ultradian rhythms in daily expression. Conclusion This study provides a first look at the chronobiological differences in gene expression between forager and nurse ant brains. This endeavor allowed us to identify a putative molecular mechanism 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 in C. floridanus , thus, likely represent a more general phenomenon that warrants further investigation.
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- Award ID(s):
- 1941546
- PAR ID:
- 10322578
- Date Published:
- Journal Name:
- BMC Genomics
- Volume:
- 23
- Issue:
- 1
- ISSN:
- 1471-2164
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1186/s12864-021-08282-x
