Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis

Zhi, Huang; Robinson, Gene E.; Tobe, Stephen S.; Yagi, Kinji; Strambi, Colette; Strambi, Alain; Stay, Barbara

doi:10.1016/0022-1910(91)90107-b

Cited by 161 publications

(123 citation statements)

References 35 publications

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“…Was this surprising? Worker behavior, including nursing and foraging, is modulated by QMP (Pankiw et al, 1998), JH (Huang et al, 1991) and ovarian Ftz-f1 and HR46 were more highly expressed in LAO than in SMO. TYR was more highly expressed in SMO than in LAO.…”

Section: Qmp Jh-ecdysteroid Hormone Axes and The Worker Ovarymentioning

confidence: 96%

Regulation of behaviorally associated gene networks in worker honey bee ovaries

Wang

Kocher

Linksvayer

et al. 2012

Journal of Experimental Biology

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Fat body expression of hormone receptor-like in 46 (HR46) and phosphoinositide-dependent kinase-1 (PDK1) correlates with ovary size as well as worker division of labor (Wang et al., 2009). HR46 is a possible nuclear hormone receptor for ecdysteroid hormones Accepted 28 September 2011 SUMMARY Several lines of evidence support genetic links between ovary size and division of labor in worker honey bees. However, it is largely unknown how ovaries influence behavior. To address this question, we first performed transcriptional profiling on worker ovaries from two genotypes that differ in social behavior and ovary size. Then, we contrasted the differentially expressed ovarian genes with six sets of available brain transcriptomes. Finally, we probed behavior-related candidate gene networks in wild-type ovaries of different sizes. We found differential expression in 2151 ovarian transcripts in these artificially selected honey bee strains, corresponding to approximately 20.3% of the predicted gene set of honey bees. Differences in gene expression overlapped significantly with changes in the brain transcriptomes. Differentially expressed genes were associated with neural signal transmission (tyramine receptor, TYR) and ecdysteroid signaling; two independently tested nuclear hormone receptors (HR46 and ftz-f1) were also significantly correlated with ovary size in wild-type bees. We suggest that the correspondence between ovary and brain transcriptomes identified here indicates systemic regulatory networks among hormones (juvenile hormone and ecdysteroids), pheromones (queen mandibular pheromone), reproductive organs and nervous tissues in worker honey bees. Furthermore, robust correlations between ovary size and neural-and endocrine response genes are consistent with the hypothesized roles of the ovaries in honey bee behavioral regulation. Supplementary material available online at

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Section: Qmp Jh-ecdysteroid Hormone Axes and The Worker Ovarymentioning

confidence: 96%

Regulation of behaviorally associated gene networks in worker honey bee ovaries

Wang

Kocher

Linksvayer

et al. 2012

Journal of Experimental Biology

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“…A worker's transition from nest tasks to foraging is mediated by decreasing Vg levels and increasing juvenile hormone (JH). Vg and JH have also been causally linked to transcriptional, physiological and metabolic changes in fat body and brain (Robinson, 1987;Huang et al, 1991;Nilsen et al, 2011;Wang et al, 2012a).…”

Section: Introductionmentioning

confidence: 99%

The gene vitellogenin affects microRNA regulation in honey bee (Apis mellifera) fat body and brain

Nunes

Ihle

Mutti

et al. 2013

Journal of Experimental Biology

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SUMMARYIn honey bees, vitellogenin (Vg) is hypothesized to be a major factor affecting hormone signaling, food-related behavior, immunity, stress resistance and lifespan. MicroRNAs, which play important roles in post-transcriptional gene regulation, likewise affect many biological processes. The actions of microRNAs and Vg are known to intersect in the context of reproduction; however, the role of these associations on social behavior is unknown. The phenotypic effects of Vg knockdown are best established and studied in the forager stage of workers. Thus, we exploited the well-established RNA interference (RNAi) protocol for Vg knockdown to investigate its downstream effects on microRNA population in honey bee foragers' brain and fat body tissue. To identify microRNAs that are differentially expressed between tissues in control and knockdown foragers, we used μParaflo microfluidic oligonucleotide microRNA microarrays. Our results showed that 76 and 74 microRNAs were expressed in the brain of control and knockdown foragers whereas 66 and 69 microRNAs were expressed in the fat body of control and knockdown foragers, respectively. Target prediction identified potential seed matches for a differentially expressed subset of microRNAs affected by Vg knockdown. These candidate genes are involved in a broad range of biological processes including insulin signaling, juvenile hormone (JH) and ecdysteroid signaling previously shown to affect foraging behavior. Thus, here we demonstrate a causal link between the Vg knockdown forager phenotype and variation in the abundance of microRNAs in different tissues, with possible consequences for the regulation of foraging behavior. Supplementary material available online at

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“…The level of juvenile hormone in the haemolymph of workers rises when they progress from performing tasks inside the colony to tasks outside the colony (Akamatsu et al 1975, Rembold 1976, Robinson 1987. Adult workers of A. mellifera present low titers of juvenile hormone in the haemolymph during the first two weeks of adult life, when they perform tasks related to brood care (Rutz et al 1976, Fluri et al 1982, and higher titers when they become foragers from the third week of life (Robinson et al 1989;Huang et al 1991Huang et al , 1994Robinson 1992). The rise in the titer of juvenile hormone induces a precocious foraging behavior (Robinson 1985, Sasagawa et al 1989, Sullivan et al 2000, thus suggesting that the mechanism through which this control is attained is through the effect of the juvenile hormone over the glandular development of the workers.…”

mentioning

confidence: 99%

Ultrastructural modifications in the venom glands of workers of Apis mellifera L. (Hymenoptera: Apidae) promoted by topical application of juvenile hormone

Roat¹,

Nocelli²,

Cruz-Landim³

2006

Neotrop. Entomol.

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Neotropical Entomology 35(2): 469-476 (2006) Modificações Ultra-Estruturais nas Glândulas de Veneno de Operárias de Apis mellifera L. (Hymenoptera:Apidae) Promovidas pela Aplicação Tópica de Hormônio Juvenil RESUMO -O presente estudo analisou, através de estudos ultra-estruturais a influência do tratamento com hormônio juvenil sobre as glândulas de veneno de operárias de Apis mellifera L. Para tanto, operárias recém-emergidas receberam aplicação tópica de 1µl de hormônio juvenil, na concentração de 2 µg/µl, sendo usado o hexano como veículo. Foram feitos dois controles, um que não recebeu nenhum tipo de tratamento (grupo C1) e o outro que recebeu aplicação tópica de 1 µl de hexano (grupo C2). O aspecto das células glandulares, em operárias recém-emergidas, mostra que estas não estão ainda secretando ativamente. Observa-se que alterações celulares ocorrem de acordo com a idade da operária e da região glandular considerada no controle C1. Assim, a fase de secreção mais ativa da glândula ocorre entre a emergência e os 14 dias de idade; aos 25 dias as células já perderam sua característica secretora, sendo a região distal a primeira a sofrer degeneração. Os tratamentos com hormônio juvenil e com hexano alteram a cronologia do ciclo glandular, antecipando o início da secreção e da degeneração da glândula. PALAVRAS-CHAVE: Ciclo secretor, degeneração glandular, hexano, abelhaABSTRACT -The present study analyzed, the influence of the treatment with juvenile hormone on the ultrastructure of Apis mellifera L. workers' venom glands. Newly emerged workers received topical application of 1 µl of juvenile hormone diluted in hexane, in the concentration of 2 µg/µl. Two controls were used; one control received no treatment (group C1) and other received topical application of 1 µl of hexane (group C2). The aspect of the glandular cells, in not treated newly emerged workers, showed that they are not yet secreting actively. Cellular modifications happened according to the worker age and to the glandular area considered. The most active phase of the gland happened from the emergence to the 14th day. At the 25th day the cells had already lost their secretory characteristic, being the distal area the first to suffer degeneration. The treatment with juvenile hormone and hexane altered the temporal sequence of the glandular cycle, forwarding the secretory cycle and degeneration of the venom gland.

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Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis

Cited by 161 publications

References 35 publications

Regulation of behaviorally associated gene networks in worker honey bee ovaries

Regulation of behaviorally associated gene networks in worker honey bee ovaries

The gene vitellogenin affects microRNA regulation in honey bee (Apis mellifera) fat body and brain

Ultrastructural modifications in the venom glands of workers of Apis mellifera L. (Hymenoptera: Apidae) promoted by topical application of juvenile hormone

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