Inactivity Is Nycthemeral, Endogenously Generated, Homeostatically Regulated, and Melatonin Modulated in a Free-Living Platyhelminth Flatworm

Abstract

Introduction: Sleep either appeared once early in the evolution of animals, or at multiple instances over evolutionary time. Understanding whether sleep is a diagnostic trait for members of the kingdom Animalia has important implications for our understanding of the evolution of sleep and sleep functions. Unfortunately, knowledge on the phylogenetic breadth of sleep is restricted to vertebrates, a few arthropods and molluscs, and one species of nematode. There is a dearth of information on the other 30 or so animal phyla.

Aims and methods: Here, we provide original data on a previously unstudied group of animals with respect to sleep: platyhelminth flatworms. These free-living animals are relatively simple, with a rudimentary central nervous system and absence of many other specialized physiological systems.

Results: Despite this simplicity, inactive flatworms appeared to be sleeping. Specifically, quiescence was organized in a circadian manner, occurring largely during the daytime. This basic rhythm persisted under constant darkness, suggesting that it was endogenously generated. Active flatworms responded more readily to stimulation, and flatworms recovered lost sleep by sleeping longer after a 3-hour period of inactivity deprivation. We were also able to increase inactivity in a dose-dependent manner with exposure to melatonin, a hormone that increases sleep in diurnal animals.

Conclusions: Taken together, these data expand our understanding of the phylogenetic extent of sleep and reinforce the idea that sleep evolved early in the evolutionary history of animals. However, additional studies on other types of animals are required for a comprehensive understanding of the origin(s) and evolution of sleep.

Keywords: Girardia tigrina; Turbellaria; evolution; function; planarian; quiescence; sleep homeostasis.