Juvenile hormone interacts with multiple factors to modulate aggression and dominance in groups of orphan bumble bee (Bombus terrestris) workers

Pandey, Anshuman; Motro, Uzi; Bloch, Guy

doi:10.1016/j.yhbeh.2019.104602

Cited by 20 publications

(35 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The evidence for modulation of circadian processes by gonadotropic hormones in insects is more ambiguous (see Introduction; Bloch et al, 2013). Here we show that JH, the major gonadotropic hormone in the bumble bee B. terrestris (Pandey et al, 2020;Shpigler et al, 2014Shpigler et al, , 2016, influences the development and strength of circadian rhythms. Notably, these findings contrast with a study with honey bees in which allatectomy and replacement therapy manipulations did not affect circadian rhythms in locomotor activity in individually isolated workers .…”

Section: Discussionmentioning

confidence: 51%

“…We thoroughly mixed the P-I, and castor oils by repeated pipetting followed by vortexing the mixture at high speed for 2-3 min. We adjusted the P-I treatment to body size (200-260µg /4.0-5.2µl castor oil/bee; Table 1), as previously reported (Pandey et al, 2020). Replacement therapy ("P-I+JH") treated bees were topically treated with P-I on Day 1, as described above.…”

Section: Manipulating Circulating Jh Titersmentioning

confidence: 99%

“…Following the P-I, and JH-III treatments, we kept the bees on ice-chilled glass plates immobilized for ~10 minutes in order to improve drug absorption and minimize possible wiping-off. Additional details on our JH manipulation procedures, and the validation of our assays, can be found in Shpigler et al, (2016) and Pandey et al, (2020).…”

Section: Manipulating Circulating Jh Titersmentioning

confidence: 99%

See 2 more Smart Citations

Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

Pandey

Motro

Bloch

2020

Preprint

Self Cite

View full text Add to dashboard Cite

The circadian and endocrine systems influence many physiological processes in animals, but little is known on the ways they interact in insects. We tested the hypothesis that juvenile hormone (JH) influences circadian rhythms in the social bumble bee Bombus terrestris. JH is the major gonadotropin in this species coordinating processes such as vitellogenesis, oogenesis, wax production, and behaviors associated with reproduction. It is unknown however, whether it also influences circadian processes. We topically treated newly-emerged bees with the allatoxin Precocene-I (P-I) to reduce circulating JH titers and applied the natural JH (JH-III) for replacement therapy. We repeated this experiment in three trials, each with bees from different source colonies. Measurements of ovarian activity confirmed that our JH manipulations were effective; bees treated with P-I had inactive ovaries, and this effect was fully reverted by subsequent JH treatment. We found that JH augments the strength of circadian rhythms and the pace of rhythm development in individually isolated newly emerged worker bees. JH manipulation did not affect the free-running circadian period, overall level of locomotor activity, or the amount of sleep. Given that acute manipulation at an early age produced relatively long-lasting effects, we propose that JH effect on circadian rhythms is mostly organizational, accelerating the development or integration of the circadian system. Sellix et al., 2004). Steroid hormones, including progestins, corticosteroids, estrogens, and androgens, were also shown to influence circadian rhythms in locomotor activity and transcription levels of core circadian clock genes in fishes (Zhao et al., 2018).The interplay between the circadian and endocrine systems is relatively little explored in adult insects (Bloch et al., 2013). Only a few studies recorded hormone titers throughout the day under constant conditions. Nevertheless, these measurements, together with indirect evidence for circadian modulation of hormone biosynthesis rate, and the expression of genes encoding proteins involved in hormone biosynthesis, hormone binding, or hormone degradation, suggest that the circadian system influences the circulating levels of many insect hormones. There is also little evidence for hormonal regulation of circadian rhythms in insects (reviewed in Bloch et al., 2013). This includes the best-studied insect hormone, juvenile hormone (JH), which functions as a gonadotropin in many insects. There is some evidence that JH and ovarian activity influences circadian rhythms in the cockroach Blattella germanica, although the data is quite perplexing. Females of this species show strong circadian rhythms during the vitellogenic phase of the reproductive cycle when JH titers are expected to be high, but not in sexually receptive females during the first gonadotropic cycle (Lee and Wu, 1994). Active ovaries mask the expression of circadian rhythms, and allatectomy abolished the strong circadian rhythms that are shown by ovariectomized female...

show abstract

Section: Discussionmentioning

confidence: 51%

Section: Manipulating Circulating Jh Titersmentioning

confidence: 99%

Section: Manipulating Circulating Jh Titersmentioning

confidence: 99%

See 1 more Smart Citation

Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

Pandey

Motro

Bloch

2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In Bombus terrestris, the best studied bumble bee, JH functions as a major gonadotropin coordinating multiple tissues and processes related to reproduction [48,[67][68][69][70][71]. This includes the expression of hundreds of brain and fat body transcripts that are differentially regulated by JH [48].…”

Section: Introductionmentioning

confidence: 99%

Krüppel-Homologue 1 Mediates Hormonally-Regulated Dominance Rank in a Social Insect

Pandey¹,

Bloch²

2021

Preprint

Self Cite

View full text Add to dashboard Cite

Dominance hierarchies are ubiquitous in invertebrates and vertebrates, but little is known on how genes influence dominance rank. Our gaps in knowledge are specifically significant concerning female hierarchies and in insects. To start filling these gaps we studied the social bumble bee Bombus terrestris, in which social hierarchies among females are common and functionally significant. Dominance rank in this bee is influenced by multiple factors, including juvenile hormone (JH) that is a major gonadotropin in this species. We tested the hypothesis that the JH responsive transcription factor Krüppel homologue 1 (Kr-h1) mediates hormonal influence on dominance behavior in the bumble bee. We first developed and validated a perfluorocarbon nanoparticles-based RNA interference protocol for knocking down Kr-h1 expression. We then used this procedure to show that Kr-h1 mediates the influence of JH not only on oogenesis and wax production, but also on aggression and dominance rank. To the best of our knowledge, this is the first study causally linking a gene to dominance rank in social insects, and one of only a few such studies in insects or in female hierarchies. These findings are important for determining whether there are general molecular principles governing dominance rank across gender and taxa.

show abstract

“…JH coordinates processes in various tissues that are 57 involved in B. terrestris reproduction including the fat body, ovaries, wax production, and exocrine gland 58 activity (Shpigler, et al 2010;Shpigler, et al 2014). JH apparently also regulates 59 processes in the central nervous system because JH manipulations affect behaviors such as dominance 60 and aggression Pandey, et al 2019). The bumble bee B. terrestris thus provides an 61 excellent contrast to honey bees to address the question of the evolutionary change in JH function 62 associated with eusociality, but little is known on the molecular processes by which JH coordinates the 63 various cells and tissues in this species.…”

mentioning

confidence: 99%

The evolution of extreme fertility defied ancestral gonadotropin mediated brain-reproduction tradeoff

Herb

Drnevich

Band

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

16Gonadotropic hormones coordinate processes in diverse tissues regulating animal reproductive 17 physiology and behavior. Juvenile hormone (JH) is the ancient and most common gonadotropin in 18 insects, but not in advanced eusocial honey bees and ants. To probe the evolutionary basis of this change, 19we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH regulated 20 processes in a bumble bee showing an intermediate level of sociliality. We found that in the fat body, 21 more JH-regulated genes were upregulated and enriched for metabolic and biosynthetic pathways. This 22 34Addressing this question is crucial for understanding both the evolution of advanced eusociality and the 51 evolution of gonadotropic hormones in general. 52To study variability in socially-related JH functions, we focused on the best-studied bumble bee, 53Bombus terrestris. Bumble bees provide an excellent model system with which to address this issue 54 because they show a simpler form of social organization relative to honey bees and ants (Wilson 1971), 55 and JH is their major gonadotropic hormone (Röseler 1977;Röseler and Röseler 1978; Bloch, Borst, et al. 56 2000;Shpigler, et al. 2014). JH coordinates processes in various tissues that are 57 involved in B. terrestris reproduction including the fat body, ovaries, wax production, and exocrine gland 58 activity (Shpigler, et al. 2010;Shpigler, et al. 2014). JH apparently also regulates 59 processes in the central nervous system because JH manipulations affect behaviors such as dominance 60 and aggression Pandey, et al. 2019). The bumble bee B. terrestris thus provides an 61 excellent contrast to honey bees to address the question of the evolutionary change in JH function 62 associated with eusociality, but little is known on the molecular processes by which JH coordinates the 63 various cells and tissues in this species. 64Here we combine hormonal manipulations, behavioral observations, and RNA sequencing 65 (RNAseq) of the brain and fat body tissues of Bombus terrestris workers. We further take advantage of 66 two "natural experiments" in which we compared gene expression in bumble bees that naturally differ in 67 JH titers. First, we analyzed the brain transcriptomes of orphan workers in which the dominant individual 68 subjected to replacement therapy show that JH regulates the expression of many genes in both the brain 126 and the fat body of bumble bee workers. 127 8 128 129 Figure 2. The effect of JH on brain gene expression. Details as in Fig 1 (A) Heat map of 3060 DEGs 130 (FDR p < 0.05) in the brain. (B) Venn diagrams comparing DEGs between the CA-treatment (left) or the 131 Sham treatment (right) and the three other treatments. (C) Three-dimensional correlation analysis for the 132 fold change expression of 700 overlapping DEGs between the CA-and the three other groups. The R 2 was

show abstract

Juvenile hormone interacts with multiple factors to modulate aggression and dominance in groups of orphan bumble bee (Bombus terrestris) workers

Cited by 20 publications

References 87 publications

Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

Krüppel-Homologue 1 Mediates Hormonally-Regulated Dominance Rank in a Social Insect

The evolution of extreme fertility defied ancestral gonadotropin mediated brain-reproduction tradeoff

Contact Info

Product

Resources

About