Molecular and Neural Mechanisms of Temperature Preference Rhythm in Drosophila melanogaster

Abstract

Temperature influences animal physiology and behavior. Animals must set an appropriate body temperature to maintain homeostasis and maximize survival. Mammals set their body temperatures using metabolic and behavioral strategies. The daily fluctuation in body temperature is called the body temperature rhythm (BTR). For example, human body temperature increases during wakefulness and decreases during sleep. BTR is controlled by the circadian clock, is closely linked with metabolism and sleep, and entrains peripheral clocks located in the liver and lungs. However, the underlying mechanisms of BTR are largely unclear. In contrast to mammals, small ectotherms, such as Drosophila, control their body temperatures by choosing appropriate environmental temperatures. The preferred temperature of Drosophila increases during the day and decreases at night; this pattern is referred to as the temperature preference rhythm (TPR). As flies are small ectotherms, their body temperature is close to that of the surrounding environment. Thus, Drosophila TPR produces BTR, which exhibits a pattern similar to that of human BTR. In this review, we summarize the regulatory mechanisms of TPR, including recent studies that describe neuronal circuits relaying ambient temperature information to dorsal neurons (DNs). The neuropeptide diuretic hormone 31 (DH31) and its receptor (DH31R) regulate TPR, and a mammalian homolog of DH31R, the calcitonin receptor (CALCR), also plays an important role in mouse BTR regulation. In addition, both fly TPR and mammalian BTR are separately regulated from another clock output, locomotor activity rhythms. These findings suggest that the fundamental mechanisms of BTR regulation may be conserved between mammals and flies. Furthermore, we discuss the relationships between TPR and other physiological functions, such as sleep. The dissection of the regulatory mechanisms of Drosophila TPR could facilitate an understanding of mammalian BTR and the interaction between BTR and sleep regulation.

Cellular and molecular organization of the Drosophila foregut

“…Body temperature regulation is mediated by Dh31/Dh31-R in Drosophila. In vertebrates, the Dh31-R ortholog, the calcitonin receptor (CalcR), controls body temperature ( 78 , 79 ). Circadian clock regulation of many aspects of animal physiology is also conserved ( 80 , 81 ).…”

Thermosensation and Temperature Preference: From Molecules to Neuronal Circuits in Drosophila

“…Both mammals and ectotherms generate BTR through behavioral strategies to regulate body temperature [110,129]. Drosophila exhibits a robust temperature preference rhythm (TPR) through which flies select a suitable environmental temperature to set their body temperature [130,131]. The TPR increases during the day, peaks in the evening, and decreases at night [130,131], suggesting that Drosophila TPR is similar to the BTR [130,131].…”

“…Drosophila exhibits a robust temperature preference rhythm (TPR) through which flies select a suitable environmental temperature to set their body temperature [130,131]. The TPR increases during the day, peaks in the evening, and decreases at night [130,131], suggesting that Drosophila TPR is similar to the BTR [130,131]. Drosophila TRP is divided into four time zones in a day: daytime zeitgeber time (ZT1-ZT12), night-onset (ZT9-ZT12, ZT13-ZT15), dark time (ZT12-ZT24), and predawn (ZT22-ZT24) [131].…”

“…The TPR increases during the day, peaks in the evening, and decreases at night [130,131], suggesting that Drosophila TPR is similar to the BTR [130,131]. Drosophila TRP is divided into four time zones in a day: daytime zeitgeber time (ZT1-ZT12), night-onset (ZT9-ZT12, ZT13-ZT15), dark time (ZT12-ZT24), and predawn (ZT22-ZT24) [131].…”

“…In a recent study by Alpert et al, the authors proposed that a subset of second-order thermosensory PNs, the TPN-II neurons, which are cold-processing neurons, projects to DN1a [142]. TPN-II could be upstream of DN1a; however, the exact role of TPN-II in TPR remains unclear [131].…”