Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants

Ju, Linyang; Glastad, Karl M.; Sheng, Lihong; Gospocic, Janko; Kingwell, Callum J.; Davidson, Shawn M.; Kocher, Sarah D.; Bonasio, Roberto; Berger, Shelley L.

doi:10.1016/j.cell.2023.08.002

Cited by 17 publications

(4 citation statements)

References 166 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Transcriptomic effects included genes related to biogenic amines, including octopamine and serotonin, and behavioral maturation-associated TFs. It would be interesting to determine whether the potent effect of this abdominal treatment on the brain is due to direct or indirect interactions; recently, it was shown that the blood–brain barrier is involved in the regulation of JH-related division of labor in Camponotus floridanus carpenter ants ( Ju et al, 2023 ).…”

Section: Discussionmentioning

confidence: 99%

Effects of microRNA-305 knockdown on brain gene expression associated with division of labor in honey bee colonies (Apis mellifera)

Stuart,

Ahmed,

Kilikevicius

et al. 2024

Journal of Experimental Biology

View full text Add to dashboard Cite

Division of labor in honey bee colonies is based on the behavioral maturation of adult workers that involves a transition from working in the hive to foraging. This behavioral maturation is associated with distinct task-related transcriptomic profiles in the brain and abdominal fat body that are related to multiple regulatory factors including juvenile hormone (JH) and queen mandibular pheromone (QMP). A prominent physiological feature associated with behavioral maturation is a loss of abdominal lipid mass as bees transition to foraging. We used transcriptomic and physiological analyses to study whether microRNAs (miRNAs) are involved in the regulation of division of labor. We first identified two miRNAs that showed patterns of expression associated with behavioral maturation, ame-miR-305-5p and ame-miR-375-3p. We then downregulated the expression of these two miRNAs with sequence-specific antagomirs. Neither ame-miR-375-3p nor ame-miR-305-5p knockdown in the abdomen affected abdominal lipid mass on their own. Similarly, knockdown of ame-miR-305-5p in combination with JH or QMP also did not affect lipid mass. By contrast, ame-miR-305-5p knockdown in the abdomen caused substantial changes in gene expression in the brain. Brain gene expression changes included genes encoding transcription factors previously implicated in behavioral maturation. The results of these functional genomic studies extend previous correlative associations of microRNAs with honey bee division of labor and point to specific roles for ame-miR-305-5p.

show abstract

Section: Discussionmentioning

confidence: 99%

Effects of microRNA-305 knockdown on brain gene expression associated with division of labor in honey bee colonies (Apis mellifera)

Stuart,

Ahmed,

Kilikevicius

et al. 2024

Journal of Experimental Biology

View full text Add to dashboard Cite

show abstract

“…Alternatively, changes in nta-1 expression in GLR may exert cell nonautonomous impacts; for example, GLR cells may regulate the local sterol hormone environment in the nerve ring during the neural circuit remodeling phase of dauer development. Recently, it has been demonstrated that glial steroid signaling in Drosophila melanogaster regulates sleep behavior ( 43 ), and glial hormone esterase governs caste-specific behavior in ants ( 44 ), indicating that the glial response to steroid hormones, which regulate plastic behavior, might be widely conserved.…”

Section: Discussionmentioning

confidence: 99%

Glial expression of a steroidogenic enzyme underlies natural variation in hitchhiking behavior

Yang,

Lee,

Kim

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Phoresy is an interspecies interaction that facilitates spatial dispersal by attaching to a more mobile species. Hitchhiking species have evolved specific traits for physical contact and successful phoresy, but the regulatory mechanisms involved in such traits and their evolution are largely unexplored. The nematode Caenorhabditis elegans displays a hitchhiking behavior known as nictation during its stress-induced developmental stage. Dauer-specific nictation behavior has an important role in natural C. elegans populations, which experience boom-and-bust population dynamics. In this study, we investigated the nictation behavior of 137 wild C. elegans strains sampled throughout the world. We identified species-wide natural variation in nictation and performed a genome-wide association mapping. We show that the variants in the promoter of nta-1 , encoding a putative steroidogenic enzyme, underlie differences in nictation. This difference is due to the changes in nta-1 expression in glial cells, which implies that glial steroid metabolism regulates phoretic behavior. Population genetic analysis and geographic distribution patterns suggest that balancing selection maintained two nta-1 haplotypes that existed in ancestral C. elegans populations. Our findings contribute to further understanding of the molecular mechanism of species interaction and the maintenance of genetic diversity within natural populations.

show abstract

“…Assessing the economical aspect of this division of labour requires measuring the physiological costs of synthesis of juvenile hormone as well as benefits of receiving it socially. Furthermore, it has been recently shown that C. floridanus have evolved a form of juvenile hormone esterase in the blood brain barrier [ 52 ] that protects individual's brains from juvenile hormone which might otherwise affect their behaviour. Potentially this enzyme might represent an adaptation to ensure worker behavioural integrity, despite the high titre of juvenile hormone that must be produced to be fed to larvae.…”

Section: Discussionmentioning

confidence: 99%

Social administration of juvenile hormone to larvae increases body size and nutritional needs for pupation

Negroni,

LeBoeuf

2023

R. Soc. open sci.

View full text Add to dashboard Cite

Social insects often display extreme variation in body size and morphology within the same colony. In many species, adult morphology is socially regulated by workers during larval development. While larval nutrition may play a role in this regulation, it is often difficult to identify precisely what larvae receive from rearing workers, especially when larvae are fed through social regurgitation. Across insects, juvenile hormone is a major regulator of development. In the ant Camponotus floridanus , this hormone is present in the socially regurgitated fluid of workers. We investigated the role the social transfer of juvenile hormone in the social regulation of development. To do this, we administered an artificial regurgitate to larvae through a newly developed handfeeding method that was or was not supplemented with juvenile hormone. Orally administered juvenile hormone increased the nutritional needs of larvae, allowing them to reach a larger size at pupation. Instead of causing them to grow faster, the juvenile hormone treatment extended larval developmental time, allowing them to accumulate resources over a longer period. Handfeeding ant larvae with juvenile hormone resulted in larger adult workers after metamorphosis, suggesting a role for socially transferred juvenile hormone in the colony-level regulation of worker size over colony maturation.

show abstract

Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants

Cited by 17 publications

References 166 publications

Effects of microRNA-305 knockdown on brain gene expression associated with division of labor in honey bee colonies (Apis mellifera)

Effects of microRNA-305 knockdown on brain gene expression associated with division of labor in honey bee colonies (Apis mellifera)

Glial expression of a steroidogenic enzyme underlies natural variation in hitchhiking behavior

Social administration of juvenile hormone to larvae increases body size and nutritional needs for pupation

Contact Info

Product

Resources

About