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J Exp Biol. 2018 Apr 12. pii: jeb.174151. doi: 10.1242/jeb.174151. [Epub ahead of print]

Thermosensory perception regulates speed of movement in response to temperature changes in Drosophila melanogaster.

Author information

1
Groningen Institute for Evolutionary Life Sciences, PO Box 11103, University of Groningen, Groningen, 9700 CC, The Netherlands.
2
Department of Cell Biology, University of Groningen, University Medical Center Groningen, A. Deusinglaan 1, 9713 AV Groningen, The Netherland.
3
Ruijsink Dynamic Engineering, Keizerstraat 57, 2801NK Gouda, The Netherlands.
4
Department of Psychology, University of Groningen, Grote Kruisstraat 2/1, 9712 TS Groningen, The Netherlands.
5
Groningen Institute for Evolutionary Life Sciences, PO Box 11103, University of Groningen, Groningen, 9700 CC, The Netherlands j.c.billeter@rug.nl.

Abstract

Temperature influences physiology and behavior of all organisms. For ectotherms, which lack central temperature regulation, temperature adaptation requires sheltering from or moving to a heat source. As temperature constrains the rate of metabolic reactions, it can directly affect ectotherm physiology and thus behavioral performance. This direct effect is particularly relevant for insects whose small body readily equilibrates with ambient temperature. In fact, models of enzyme kinetics applied to insect behavior predict performance at different temperatures, suggesting that thermal physiology governs behavior. However, insects also possess thermosensory neurons critical for locating preferred temperatures, showing cognitive control. This suggests that temperature-related behavior can emerge directly from a physiological effect, indirectly as consequence of thermosensory processing, or through both. To separate the roles of thermal physiology and cognitive control, we developed an arena that allows fast temperature changes in time and space, and in which animals' movements are automatically quantified. We exposed wild-type and thermosensory receptor mutants Drosophila melanogaster to a dynamic temperature environment and tracked their movements. The locomotor speed of wild-type flies closely matched models of enzyme kinetics, but the behavior of thermosensory mutants did not. Mutations in thermosensory receptor dTrpA1 (Transient receptor potential) expressed in the brain resulted in a complete lack of response to temperature changes, while mutation in peripheral thermosensory receptor Gr28b(D) resulted in diminished response. We conclude that flies react to temperature through cognitive control, informed by interactions between various thermosensory neurons, whose behavioral output resembles that of enzyme kinetics.

KEYWORDS:

Drosophila melanogaster; Locomotor activity; Temperature; Thermal performance; Thermosensory receptors

PMID:
29650755
DOI:
10.1242/jeb.174151

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