Decoding the evolutionary genetics of sleep and nocturnality

Many of the mechanisms that regulate the phase, duration, and structure of sleep are conserved, yet paradoxically, sleep displays remarkable variation both across and within species. Animals can have different chronotypes (‘early-birds’/‘night-owls’) or spend variable amounts of time asleep (2-18hrs/day). Species can shift the phase of their activity (nocturnal/diurnal), restrict activity to specific periods (dawn/dusk), or lose rhythmicity entirely. In my research program, I use fish models to study the genomic and cellular mechanisms underlying sleep diversity. Using single-cell sequencing from zebrafish and the insomniac Mexican cavefish we identified cell types and genomic signatures coincident with the loss of sleep, and general principles underlying cell-type evolution in the vertebrate brain (Shafer et. al. Nature Ecology & Evolution, 2021). To study the evolution of sleep diversity beyond its loss, I have launched a large-scale behavioural screen of the hyperdiverse African cichlid fishes. This screen establishes cichlids as a powerful new model clade to uncover the genetic basis of sleep variation. Analysis of >70 species has uncovered that cichlids occupy all circadian niches (diurnal, nocturnal, crepuscular, and arrhythmic) and display variation in where and how much they sleep (2-18hrs/day). This variation is equivalent to that observed across all mammals, yet cichlids are as closely related as chimpanzees and humans, enabling identification of genes responsible for behaviours. Indeed, GWAS of sleep-related behaviours in cichlids revealed an unexpected enrichment for genes associated with human neuropsychiatric disorders rather than the circadian clock. In parallel I have generated a database of the diurnal activity patterns of >4000 species of fish, spanning over 300 my of evolution. These data indicate that the last common ancestor of all fish was nocturnal, and that fish have undergone twice as many transitions between nocturnality and diurnality than any other vertebrate group. In the future I will use micro- (cichlids) and macro- (all fish) evolutionary approaches to dissect the genomics and evolution of sleep diversity. If you would like to meet with Max after his seminar, please contact nicholas.provart@utoronto.ca.