Academic journal article Genetics

Quantitative Genetic Analysis of Sleep in Drosophila Melanogaster

Academic journal article Genetics

Quantitative Genetic Analysis of Sleep in Drosophila Melanogaster

Article excerpt

ABSTRACT

Although intensively studied, the biological purpose of sleep is not known. To identify candidate genes affecting sleep, we assayed 136 isogenic P-element insertion lines of Drosophila melanogaster. Since sleep has been negatively correlated with energy reserves across taxa, we measured energy stores (whole-body protein, glycogen, and triglycerides) in these lines as well. Twenty-one insertions with known effects on physiology, development, and behavior affect 24-hr sleep time. Thirty-two candidate insertions significantly impact energy stores. Mutational genetic correlations among sleep parameters revealed that the genetic basis of the transition between sleep and waking states in males and females may be different. Furthermore, sleep bout number can be decoupled from waking activity in males, but not in females. Significant genetic correlations are present between sleep phenotypes and glycogen stores in males, while sleep phenotypes are correlated with triglycerides in females. Differences observed in male and female sleep behavior in flies may therefore be related to sex-specific differences in metabolic needs. Sleep thus emerges as a complex trait that exhibits extensive pleiotropy and sex specificity. The large mutational target that we observed implicates genes functioning in a variety of biological processes, suggesting that sleep may serve a number of different functions rather than a single purpose.

UNLIKE many behaviors, the biological purpose of sleep remains elusive. Yet sleep is thought to serve an important physiological function for two reasons: it has been observed in a wide variety of taxa (Amlaner and Ball 1994; Hartse 1994; Zepelin 1994), and animals deprived of sleep suffer severe physical consequences, including death (Rechtschaffen et al. 1989; Rechtschaffen and Bergmann 2002). Diverse hypotheses have been postulated about the function of sleep. A number of proposals stem from the negative correlation observed between sleep and body weight across mammalian species (Zepelin 1994). Since animals with lower energy reserves tend to sleep more, sleep might serve the purpose of reducing total caloric expenditure, thereby conserving energy (Zepelin 1994; Berger and Phillips 1995). Studies of sleep deprivation in humans tend to support the idea that sleep plays a role in metabolism: sleep loss results in impaired glucose tolerance (Spiegel et al. 1999) and changes in appetite-stimulating/suppressing hormones such as leptin and ghrelin (Spiegel et al. 2004a,b). Furthermore, a widespread association between short sleep times and obesity has been observed in humans (reviewed in Cizza et al. 2005). However, few calories are saved by sleeping vs. quiet waking (Zepelin 1994), implying that the loss of consciousness is central to the function of sleep. A number of hypotheses therefore argue that sleep is primarily for the benefit of the brain. Sleep may restore brain glycogen,animportant source of metabolic energy (Benington and Heller 1995). In addition, sleepmaybe required for synaptic plasticity (Tononiand Cirelli 2003). Waking activities that result in cellular changes in the brain increase the strength of wake-active synapses; slow-wave activity during sleep may serve to downscale synaptic strength, thus improving performance (Tononi and Cirelli 2003). Or sleep may stimulate neurons that were not sufficiently activated in the course of waking, as a means of preserving information (Krueger et al. 1995). Sleep has also been associated with the process of memory consolidation in mammals (Smith 1995); while sleep does not appear to affect all types of memory, nondeclarative memories such as motor learning tasks are enhanced by a night of sleep (Stickgold 2005). Each theory cited above has been supported to some degree by experimental evidence. Sleep thus emerges as a complex behavior that may serve more than one purpose.

Quiescence in the fruit fly Drosophila melanogaster possesses all of the behavioral characteristics of mammalian sleep (Hendricks et al. …

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