Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila

Abstract

Like other ectotherms, the roundworm Caenorhabditis elegans and the fruit fly Drosophila melanogaster rely on behavioral strategies to stabilize their body temperature. Both animals use specialized sensory neurons to detect small changes in temperature, and the activity of these thermosensors governs the neural circuits that control migration and accumulation at preferred temperatures. Despite these similarities, the underlying molecular, neuronal, and computational mechanisms responsible for thermotaxis are distinct in these organisms. Here, we discuss the role of thermosensation in the development and survival of C. elegans and Drosophila, and review the behavioral strategies, neuronal circuits, and molecular networks responsible for thermotaxis behavior.The ability to sense and respond to ambient temperature is crucial for the survival and fitness of all animals. Endotherms such as birds and mammals maintain a relatively constant body temperature regardless of ambient temperature via a number of mechanisms, including behavioral modification, as well as central regulation of autonomic nervous system functions (Hensel 1973;Simon et al. 1986). However, for ectotherms like Caenorhabditis elegans and Drosophila melanogaster, whose body temperature varies with ambient temperature, behavioral strategies are the primary mechanism for regulating optimal internal temperature (Stevenson 1985;Huey et al. 2003). In this review, we describe the known neuronal and molecular strategies used by C. elegans and Drosophila to detect and behaviorally respond to changes in temperature, focusing particularly on temperatureguided behaviors that operate within each animal's normal thermal zone. A note on terminologyVarious terms have been used to describe patterns of thermotactic movement in C. elegans and Drosophila. For instance, worms moving down temperature gradients toward cooler temperatures are said to be ''cryophilic'' (Fig. 1A), while the same behavior executed by flies is called ''warmth avoidance.'' By the same logic, movements up temperature gradients have been called ''thermophilic'' in worms and ''cold avoidance'' behavior in flies (Fig. 1B). Here, movement down and up temperature gradients will be referred to as ''negative thermotaxis'' and ''positive thermotaxis,'' respectively. In addition to positive and negative thermotaxis, worms have a robust tendency to move along isothermal contours when they are near their preferred temperature, a behavior referred to as ''isothermal tracking'' (Fig. 1E). Isothermal tracking has not been observed in flies. The ethology of thermotaxis in C. elegans and D. melanogasterTemperature is an environmental variable that affects the rate and nature of all chemical reactions, and hence has dramatic effects on animal physiology. At the extremes of the temperature spectrum, exposure to excessive heat or cold causes dramatic perturbations in cellular physiology that rapidly lead to the failure of nervous system function and to serious tissue damage. Thus, thermal nociception-the ability to ...

GCY-8, PDE-2, and NCS-1 are critical elements of the cGMP-dependent thermotransduction cascade in the AFD neurons responsible for C. elegans thermotaxis

“…This study concerns the AFD neurons, whose sensory dendrites terminate in a specialized ending comprised of a primary cilium and an extensive array of microvilli (Ward et al, 1975;White et al, 1986). At least five genes are known to be essential for thermotransduction by AFD (Garrity et al, 2010): tax-4 and tax-2, which encode the  and  subunits of a CNG ion channel, and gcy-8, gcy-18, and gcy-23, which encode receptor guanylate cyclases (rGCs) and are exclusive to the AFD neurons. Warming-evoked thermoreceptor currents (ThRCs) in AFD are carried by a nonselective cation channel that depends on tax-4 and tax-2 (Ramot et al, 2008a).…”

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

“…The nematode worm Caenorhabditis elegans represents a valuable model system for exploring the molecular and cellular underpinnings of these two fundamental questions. Many studies of C. elegans behavior (for example, chemotaxis, thermotaxis, and mechanosensation) use hermaphrodites in simple behavioral assays (for review, see Bargmann, 2006;Goodman, 2006;Garrity et al, 2010). These behaviors are mediated by relatively few sensory receptor cells with limited in-built redundancy (Chalfie and Sulston, 1981;Bargmann and Horvitz, 1991;Biron et al, 2008).…”

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

“…Moreover, the simpler body plan and crawling movements of the larva facilitate the precise quantification of behavioral dynamics. Poikilotherms like C. elegans or Drosophila use sensitive thermosensory mechanisms to navigate moderate temperature ranges, thereby enabling them to use their environments to regulate their own body temperatures (3,4). Here, we study sensory and behavioral dynamics during positive thermotaxis (i.e., cool avoidance) by the Drosophila larva.…”