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

Abstract

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...