Sexual dimorphism of sleep regulated by juvenile hormone signaling in Drosophila

Abstract

Sexually dimorphic phenotypes are a universal phenomenon in animals. In the model animal fruit fly Drosophila, males and females exhibit long- and short-sleep phenotypes, respectively. However, the mechanism is still a mystery. In this study, we showed that juvenile hormone (JH) is involved in regulation of sexually dimorphic sleep in Drosophila, in which gain of JH function enlarges differences of the dimorphic sleep phenotype with higher sleep in males and lower sleep in females, while loss of JH function blurs these differences and results in feminization of male sleep and masculinization of female sleep. Further studies indicate that germ cell-expressed (GCE), one of the JH receptors, mediates the response in the JH pathway because the sexually dimorphic sleep phenotypes cannot be rescued by JH hormone in a gce deletion mutant. The JH-GCE regulated sleep dimorphism is generated through the sex differentiation-related genes -fruitless (fru) and doublesex (dsx) in males and sex-lethal (sxl), transformer (tra) and doublesex (dsx) in females. These are the “switch” genes that separately control the sleep pattern in males and females. Moreover, analysis of sleep deprivation and circadian behaviors showed that the sexually dimorphic sleep induced by JH signals is a change of sleep drive and independent of the circadian clock. Furthermore, we found that JH seems to also play an unanticipated role in antagonism of an aging-induced sleep decrease in male flies. Taken together, these results indicate that the JH signal pathway is critical for maintenance of sexually dimorphic sleep by regulating sex-relevant genes.

Social behavior and aging: A fly model

“…214 The expression of some genes involved in courtship also change with aging. 220 The effect of aging on sex-specific transcription factors is a potential mechanism for sex differences in aging. They are thought to be important in early adult development, such as for proper pigment allocation, and thus may have reduced importance later in life.…”

“…Since this gene has alternative splicing, this effect is most likely to be mediated by the fru transcript that encodes a male-specific transcription factor. 220 The effect of aging on sex-specific transcription factors is a potential mechanism for sex differences in aging.…”

Evolution of Reproductive Behavior

“…Thus, a precondition for any behavior to evolve is that there is genetic variation for the behavior within the population. The DGRP and other resources mentioned above have revealed extensive natural variation for behavioral phenotypes (Brown et al 2013;Harbison et al 2013;Swarup et al 2013;Appel et al 2015;Arya et al 2015;Ayroles et al 2015;Garlapow et al 2015;Shorter et al 2015;Carbone et al 2016;Rohde et al 2017;Wu et al 2018a), including reproductive behaviors (Turner et al 2013;Gaertner et al 2015). The genetic architectures underlying behaviors are often complex, allowing very fine-grained effects when selective forces result in the redistribution of allele frequencies leading to modifications of the genetic networks that orchestrate the behavior.…”

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

“…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.…”

“…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).…”