Social Experience Is Sufficient to Modulate Sleep Need of Drosophila without Increasing Wakefulness

Abstract

Organisms quickly learn about their surroundings and display synaptic plasticity which is thought to be critical for their survival. For example, fruit flies Drosophila melanogaster exposed to highly enriched social environment are found to show increased synaptic connections and a corresponding increase in sleep. Here we asked if social environment comprising a pair of same-sex individuals could enhance sleep in the participating individuals. To study this, we maintained individuals of D. melanogaster in same-sex pairs for a period of 1 to 4 days, and after separation, monitored sleep of the previously socialized and solitary individuals under similar conditions. Males maintained in pairs for 3 or more days were found to sleep significantly more during daytime and showed a tendency to fall asleep sooner as compared to solitary controls (both measures together are henceforth referred to as “sleep-enhancement”). This sleep phenotype is not strain-specific as it is observed in males from three different “wild type” strains of D. melanogaster. Previous studies on social interaction mediated sleep-enhancement presumed ‘waking experience’ during the interaction to be the primary underlying cause; however, we found sleep-enhancement to occur without any significant increase in wakefulness. Furthermore, while sleep-enhancement due to group-wise social interaction requires Pigment Dispersing Factor (PDF) positive neurons; PDF positive and CRYPTOCHROME (CRY) positive circadian clock neurons and the core circadian clock genes are not required for sleep-enhancement to occur when males interact in pairs. Pair-wise social interaction mediated sleep-enhancement requires dopamine and olfactory signaling, while visual and gustatory signaling systems seem to be dispensable. These results suggest that socialization alone (without any change in wakefulness) is sufficient to cause sleep-enhancement in fruit fly D. melanogaster males, and that its neuronal control is context-specific.

Contribution of Social Influences through Superposition of Visual and Olfactory Inputs to Circadian Re-entrainment

“…In summary, we have shown that interactions with WT flies partially rescue re-entrainment deficiency in jet c and cry b mutants, as measured by locomotor activity. Previous works suggest that olfactory signaling mediates social entrainment in flies (Eban-Rothschild and Bloch, 2012;Fujii and Amrein, 2010;Fujii et al, 2007;Levine et al, 2002;Lone et al, 2016;Lone and Sharma, 2012). In contrast, we found that both visual and olfactory inputs significantly contributed to re-entrainment.…”

“…Although Drosophila melanogaster is classified as a solitary species, these flies aggregate at high densities to feed and they exhibit social entrainment, aggression, and collective behavior (Levine et al, 2002;Liu et al, 2011;Ramdya et al, 2015;Schneider et al, 2012;Veenema, 2009;Wang and Anderson, 2010). Studies using Drosophila have begun to define the molecular and neuronal mechanisms controlling social entrainment (Bloch et al, 2013;Fujii and Amrein, 2010;Fujii et al, 2007;Levine et al, 2002;Lone et al, 2016;Lone and Sharma, 2012). In particular, volatile pheromones, the olfactory system, and some clock neurons are involved.…”

The Effect of Mating and the Male Sex Peptide on Group Behaviour of Post-mated Female Drosophila melanogaster

“…Previous studies have shown that socially enriched individuals sleep more compared to flies that are socially deprived [48,50]. These studies focused on the social experience prior to the monitoring of sleep and wakeful activity in individual flies and therefore differed from the present study and that of Liu et al [49], who studied social behaviour in populations where flies experience ongoing interactions with other members of the community.…”

Regulation of Social Stress and Neural Degeneration by Activity-Regulated Genes and Epigenetic Mechanisms in Dopaminergic Neurons

“…Such long-lasting but ultimately reversible state changes in Drosophila usually involve various neuropeptides [ 9 , 10 ] and neurotransmitters including dopamine [ 5 , 11 , 12 ]. Prolonged social isolation in Drosophila can drastically affect behavior as in mammals; for instance, socially isolated Drosophila show a reduction in sleep [ 13 , 14 ] and an increase in aggression [ 15 , 16 ], both modulated by DAN signaling.…”