Divergent evolution of sleep functions
Elephants spend up to 18 hours a day eating grass, bushes, roots, shrubs to maintain their appropriate calorie intake. They sleep only 1 or 2 hours a day. Bats, on the other hand, are believed to sleep more than 20 hours a day. Finally, Great Frigatebird. They would normally sleep 9-10 hours a day and you would have hard time trying to get them to sleep less than that. Unless it’s migratory season. In that case, they sleep 40 minutes a day, while they flies for days and days in a row. Evolution is one of the great mysteries of sleep. Why do some animals require 20 hours, while others can cope with 1 or 2? Whatever sleep function is, how can it be accomplished in 10 hours in one season and 40 minutes in another, as it happens in migratory birds?
We won’t really understand what sleep is and what it does if we keep thinking about it in an anthropocentric way. We need to look at it from the evolutionary standpoint and only then we will be able to grasp what its role in nature is. This work marks our first big attempt in this direction. We did not compare sleep between elephants and bats. Too tricky to keep in the test tube and too evolutionary distant. Instead, we used seven species of Drosophila spanning an evolutionary distance of 5-50 Million years and with different ancestral origins and adaptation niches.
In all of them, we measure sleep using a computerised video tracking system based on Raspberry PIs which can be linked to robots to deliver sensory stimuli in real-time, such as puffs of air or automatic rotations of the test tube to keep them awake. We had actually used this device before to explore how fruitflies recognise and respond to salient stimuli during sleep. Here, we combined those with the excellent hidden Markov chain model initially proposed by the Griffith Lab at Brandeis and were able to confirm that different sleep stages as detected by the Markov chain do indeed coincide with different arousabilities. Deep sleeping flies are harder to wake up!
We found that all species sleep in more or less the same way, although for very different lengths of time. In almost all species, sleep is sexually dimorphic: females sleep only at night and males sleep in the afternoon too. Except for D. virilis: a cosmopolitan species believed to have arisen in the Miocene in the deserts of Afghanistan. Interestingly, this is something very recently found in other desert species too. You probably don’t want to be flying around in a desertic afternoon! So, sleep amount is generally conserved and obviously it adapts to species-specific ecological conditions, exactly as for the elephant and the bat. But what about sleep homeostasis? How do these exotic flies react when we try to keep them awake? For this, we turned to our trusty robots and kept flies awake for 24 hours in a row by rotating their little world around every time the fell asleep. A bit like in the Inception movie. Watch the first tube from the left to see the robot in action.
When you deprive an animal of sleep, it tries to recover some of it ASAP. This is a hallmark of sleep homeostasis and what we observed in D. melanogaster, but not in any of the other species! Like the migratory birds, they suddenly seemed OK not sleeping. No signs of tiredness. And even making our robot work for 7 days in a row – 168 hours – did nothing to them! These other species could stay awake just fine and showed no signs of tiredness. Except for melanogaster, which showed a steady increase in sleep pressure. However, at least some species were able to show rebound sleep when we used a different way of keeping them awake: social stress induced by male-male interaction in a laboratory boxing-ring equivalent. Stress can induce rebound sleep in many species, including rodents, and it does so by activating specific brain circuits as our colleagues recently showed.
Surprisingly, male-male interaction did lead to sleep rebound not just in melanogaster but also, simulans, sechelia, yakuba. Still no signs of homeostasis in the remaining three species though! What decides whether an animal will show homestasis? It seems the answer is in their brains. We found that, in general, sleep rebound correlated with an increase in synaptic strength. All the flies that showed rebound also showed a larger amount of a specific synaptic protein. And conversely, when we remove synaptic proteins from specific parts of the brain involved in learning and memory in D. melanogaster we get a similar effect: no tiredness after sleep deprivation.
We also go on and look at the evolution of pharmacology in these species and much more. Have a go at the manuscript yourself. It’s hopefully easy to read for everyone. hat is the take-home message? Well, we try to figure out what all this means in evolutionary terms. We think sleep has different functions in different species (doh!) and some functions therefore evolved for some species but not others. The one common thing all animals have in common is they all sit on the same planet which has been rotating at the same speed for a very long time. We believe this adaptation created sleep in the first place giving animals a chance to optimise their activities to days & nights. Then, other sleep functions kicked in. Some animals need sleep to cope with stress; some others need sleep to learn better; to memorize; to fight bacteria. Who knows how many different functions there are? Some need sleep for multiple reasons at once. This makes sense on multiple levels and can ultimately explain why elephants can do in 1 hour what bats seem to take 20 hours for!