Divergent evolution of sleep functions

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Abstract

Most living organisms have evolved to synchronize their biological activities with the earth’s rotation, a daily regulation of biology and behaviour controlled by an evolutionary conserved molecular machinery known as the circadian clock. For most animals, circadian mechanisms are meant to maximize their exposure to positive activities ( e.g.: social interactions, mating, feeding – generally during the day) and minimize their exposure to peril ( e.g.: predation, weather, darkness – generally during the night 1 ). On top of circadian regulation, some behaviours also feature a second layer of homeostatic control acting as a fail-safe to ensure important activities are not ignored. Sleep is one of these behaviours: largely controlled by the circadian clock for its baseline appearance, it is at the same time modulated by a – poorly understood – homeostatic regulator ensuring animals obey their species-specific amount of daily sleep 2 . An evolutionary conserved homeostatic control is often considered the main evidence for a core biological function of sleep beyond the trivial one (that is: keeping us out of trouble by limiting our energy expenditure and exposure to danger 3,4 ) and it is hypothesized that sleep evolved around this mysterious basic biological function. Here we characterize sleep regulation in a group of seven species of the Drosophila genus at key evolutionary distances and representing a variety of ecological niche adaptations. We show that the spontaneous circadian-driven aspects of sleep are conserved among all species but the homeostatic regulation, unexpectedly, is not. We uncover differences in the behavioural, cell-biological and neuro-pharmacological aspects of sleep and suggest that, in Drosophilids, sleep primarily evolved to satisfy a circadian role, keeping animals immobile during dangerous hours of the day. The homeostatic functions of sleep evolved independently, in a species-specific fashion, and are not conserved.

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  1. To investigate how profound is the evolutionary conservation of sleep in Drosophilids, we created anovel paradigm for the analysis of sleep depth

    I would re-phrase this sentence. :)

  2. c

    It would be interesting to think about how we can point to biological/neurological associations with sleep changes without referring to previous work that discovered those associations. I.e Could a tool like NovelTree point to the four genes involved in synaptic plasticity that you’ve tested as potential drivers of the difference in sleep rebound phenotypes or perhaps reveal other unknown gene associations? NovelTree Pipeline: doi.org/10.57844/arcadia-z08x-v798

  3. a

    Even though rebound sleep wasn’t seen during the ZT 0-3 state for species other than D. melanogaster, there does seem to be an increase in sleep during the “natural sleep period” (ZT 12-24 state) for D. erecta, D. yakuba and D. willinstoni. Do you think it is possible that a rebound response could occur much later in the next sleep cycle rather than immediately after sleep disruption ends?

  4. e

    The sexual dimorphism here is fascinating, especially because this is also seen in human sleep-wake disorders! For example, insomnia is more prevalent among women than among men and the discrepancy becomes larger with age. Did you consider comparisons between sex for any of the species other than D. virilis? Perhaps looking at the same species could serve as a useful control for ecological and dietary impacts?

  5. a

    Perhaps this is difficult due to an experimental limitation but it could have been nice to include another Drosophila species with a vegetable ecological niche for your analysis. D. mojavensis could be especially useful since it has a similar “siesta” sleep phenotype as D. virilis and I would be curious to see if it also shows a lack of sexual dimorphism and no sleep rebound differences as well.