Brain gene expression analyses in virgin and mated queens of fire ants reveal mating‐independent and socially regulated changes

Abstract

Transcriptomes of dissected brains from virgin alate and dealate mated queens from polygyne fire ants (Solenopsis invicta) were analyzed and compared. Thirteen genes were upregulated in mated queen brain, and nine were downregulated. While many of the regulated genes were either uncharacterized or noncoding RNAs, those annotated genes included two hexamerin proteins, astakine neuropeptide, serine proteases, and serine protease inhibitors. We found that for select differentially expressed genes in the brain, changes in gene expression were most likely driven by the changes in physiological state (i.e., age, nutritional status, or dominance rank) or in social environment (released from influence of primer pheromone). This was concluded because virgins that dealated after being separated from mated queens showed similar patterns of gene expression in the brain as those of mated queens for hexamerin 1, astakine, and XR_850909. Abaecin (XR_850725), however, appears upregulated only after mating. Therefore, our findings contribute to distinguish how specific gene networks, especially those influenced by queen primer pheromone, are regulated in queen ants. Additionally, to identify brain signaling pathways, we mined the fire ant genome and compiled a list of G‐protein‐coupled receptors (GPCRs). The expression level of GPCRs and other genes in the “genetic toolkit” in the brains of virgin alates and mated dealate queens is reported.

Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques

“…Together, our results dovetail with those from eusocial insects [honey bees and ants: (71–74)], sticklebacks and cichlid fish (18, 60, 75, 76), and rodents (61, 77, 78) to emphasize the importance of social modulation of gene regulation, including both gene expression levels and epigenetic states. Our findings specifically reinforce the role of social interactions in immune cell gene regulation, building substantially on our prior work (9, 10) by revealing a key role for chromatin dynamics and accessibility to TF binding.…”

Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?

“…By targeting the most relevant sensory organ associated with this behavior, our study provided better sensitivity to detect tissue-specific differences compared to similar studies which used the whole bodies of workers (Wang et al, 2008) and queens (Nipitwattanaphon, Wang, Dijkstra, & Keller, 2013). Other transcriptomics experiments have been conducted in fire ants in other contexts (Calkins et al, 2018;Chen, Shen, & Lee, 2006;Morandin et al, 2016;Nipitwattanaphon et al, 2014;Qiu et al, 2018). Our results and follow-up experiments uncovered an interesting, differentially expressed OBP, SiOB12b′, whose expression patterns suggest that it may play a role in the differences between monogyne and polygyne colony forms in fire ants.…”

Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta)

“…Further, in contrast to worker bees, none of the four Vg genes were regulated in workers by topical application of the JH-analog S-hydroprene [10]. In a different study, we have shown that when comparing brain transcriptomes of alate virgin and dealate mated queens, the expression of two hexamerins, hexamerin-like (LOC105192919, hereafter called hexamerin 1 ) and arylphorin subunit alpha-like (LOC105192898), is significantly reduced in brains of mated queens [41]. In the same transcriptome analysis, no differences in expression were observed for the other two hexamerin genes, hexamerin (LOC105204474, hereafter called hexamerin 2 ) and arylphorin subunit beta (LOC105192897).…”