foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila

Abstract

Recent human studies suggest that genetic polymorphisms allow an individual to maintain optimal cognitive functioning during sleep deprivation. If such polymorphisms were not associated with additional costs, selective pressures would allow these alleles to spread through the population such that an evolutionary alternative to sleep would emerge. To determine whether there are indeed costs associated with resiliency to sleep loss, we challenged natural allelic variants of the foraging gene (for) with either sleep deprivation or starvation. Flies with high levels of Protein Kinase G (PKG) (for R ) do not display deficits in short-term memory following 12 h of sleep deprivation. However, short-term memory is significantly disrupted when for R flies are starved overnight. In contrast, flies with low levels of PKG (for s , for s2 ) show substantial deficits in short-term memory following sleep deprivation but retain their ability to learn after 12 h of starvation. We found that for R phenotypes could be largely recapitulated in for s flies by selectively increasing the level of PKG in the α/β lobes of the mushroom bodies, a structure known to regulate both sleep and memory. Together, these data indicate that whereas the expression of for may appear to provide resilience in one environmental context, it may confer an unexpected vulnerability in other situations. Understanding how these tradeoffs confer resilience or vulnerability to specific environmental challenges may provide additional clues as to why an evolutionary alternative to sleep has not emerged.A lthough sleep is a behavioral state that is conserved across a diverse range of species, the biological functions of sleep remain unknown. Sleep deprivation (SD) has been shown to negatively impact cognition, but individual responses to sleep loss can vary significantly within a population (1). Recent studies suggest that a portion of this variability may be influenced by genetic factors (2). For example, polymorphisms for PERIOD 3 (PER3), a circadian clock gene, can predict the magnitude of cognitive impairment and sleep homeostasis in response to a night of SD in humans (2). Although these genetic contributions may attenuate impairments following SD, the tradeoffs associated with resistance to sleep loss remain unknown. Presumably, the potential costs must be substantial. Thus, it is likely that the price of protection from sleep loss that can be conferred by allelic variation in one environment may induce a cost when manifested in a different environment. To date, putative costs of resiliency to sleep loss have not been identified in humans or any model organism.foraging (for), which codes for Protein Kinase G (PKG), is maintained in wild-type populations as a genetic polymorphism that results in either higher or lower levels of PKG activity (3). The allele associated with higher levels of PKG ("rover"; for R ) results in larvae with longer foraging trails between food patches, whereas the allele associated with lower levels of PKG ("sitter"; for s ) results i...

Sleep Restores Behavioral Plasticity to Drosophila Mutants

“…We have previously shown that sleep supports LTM using courtship conditioning [23, 31, 54, 55]. Thus, we asked whether THIP-induced sleep would restore LTM to rut 2080 mutants.…”

“…Flies lacking the male-specific fruitless gene ( fruM ) will court if they have been grouped with other flies for several days [70]. Mutations in the foraging gene ( for s2 ) have impaired STM, but these deficits can be reversed following a brief period of starvation [54]. Finally, circuit specific deficits in LTM as assessed using courtship conditioning can be reversed when the same flies are evaluated in the absence of visual input [71].…”

Gene–environment interplay inDrosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

“…To determine the effect of for expression in the MBs on open-field behavior, we used UAS and Gal4 constructs (56) crossed into a white 1 (w 1 ) sitter (for s ) genetic background. The three Gal4 driver lines were as follows: 30Y-Gal4, which expresses in all MB lobes (α, α′, β, β′, and γ); c739-Gal4, which expresses in the α-and β-lobes and Kenyon cells; and 201Y-Gal4, which expressed strongly in the γ-lobes and more weakly in the α-and β-lobes (21,22,55). Transgenic expression of for was accomplished with a w 1 ;for s ;UASforT1a line (21).…”

“…The three Gal4 driver lines were as follows: 30Y-Gal4, which expresses in all MB lobes (α, α′, β, β′, and γ); c739-Gal4, which expresses in the α-and β-lobes and Kenyon cells; and 201Y-Gal4, which expressed strongly in the γ-lobes and more weakly in the α-and β-lobes (21,22,55). Transgenic expression of for was accomplished with a w 1 ;for s ;UASforT1a line (21). We crossed this UAS-forT1a line with the Gal4 lines and tested the female progeny in the open field.…”

Altered regulation of sleep and feeding contribute to starvation resistance in Drosophila

“…Although functional interactions between foraging and sleep have been described, the evolutionary trade-offs between these behaviors has been difficult to test experimentally. Both sleep and feeding are highly variable in Drosophila, and naturally occurring polymorphisms have been identified that modulate the interaction between these processes (Kaun et al, 2007;Keene et al, 2010;McDonald and Keene, 2010;Donlea et al, 2012).…”