Abstract

Drosophila third-instar larvae exhibit changes in their behavioral responses to gravity and food as they transition from feeding to wandering stages. Using a thermal gradient encompassing the comfortable range (18°C to 28°C), we found that third-instar larvae exhibit a dramatic shift in thermal preference. Early third-instar larvae prefer 24°C, which switches to increasingly stronger biases for 18°C-19°C in mid- and late-third-instar larvae. Mutations eliminating either of two rhodopsins, Rh5 and Rh6, wiped out these age-dependent changes in thermal preference. In larvae, Rh5 and Rh6 are thought to function exclusively in the light-sensing Bolwig organ. However, the Bolwig organ was dispensable for the thermal preference. Rather, Rh5 and Rh6 were required intrpA1-expressing neurons in the brain, ventral nervecord, and body wall. Because Rh1 contributes tothermal selection in the comfortable range during the early to mid-third-instar stage, fine thermal discrimination depends on multiple rhodopsins.

Highlights

  • The capacity to sense and avoid acute exposure to noxious heat and cold is critical for survival, and in many animals, this ability depends on direct activation of transient receptor potential (TRP) channels (Julius, 2013; Venkatachalam and Montell, 2007)

  • Drosophila can respond behaviorally to thermal fluctuations of a fraction of a degree (Fowler and Montell, 2013; Klein et al, 2015). This is best documented in Drosophila larvae (Klein et al, 2015), and we have shown previously that the exquisite sensitivity to small changes in temperature in the comfortable range depends on a thermosensory signaling cascade that is initiated by one of the seven rhodopsins (Rh1) (Kwon et al, 2008; Shen et al, 2011)

  • To mid-third-instar larvae are motivated by feeding, while the late-third-instar larvae must prepare for the final, wandering stage, when they escape from food and subsequently pupate

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Summary

Introduction

The capacity to sense and avoid acute exposure to noxious heat and cold is critical for survival, and in many animals, this ability depends on direct activation of transient receptor potential (TRP) channels (Julius, 2013; Venkatachalam and Montell, 2007). Animals ranging from worms to humans are sensitive to small temperature differences in the comfortable range and respond by selecting their preferred temperature zones (Julius, 2013; Venkatachalam et al, 2014; Venkatachalam and Montell, 2007). This behavior is especially acute in poikilothermic organisms such as the fruit fly, Drosophila melanogaster, which equilibrates its body temperature with the environment. It was unclear whether third-instar larvae exhibit major changes in thermal preference before entering the wandering stage

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