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The evolution of cold nociception in drosophilid larvae and identification of a neural basis for cold acclimation

View ORCID ProfileNathaniel J. Himmel, View ORCID ProfileJamin M. Letcher, View ORCID ProfileAkira Sakurai, View ORCID ProfileThomas R. Gray, Maggie N. Benson, View ORCID ProfileKevin J. Donaldson, View ORCID ProfileDaniel N. Cox
doi: https://doi.org/10.1101/2021.01.04.425280
Nathaniel J. Himmel
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Jamin M. Letcher
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Akira Sakurai
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Thomas R. Gray
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Maggie N. Benson
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Kevin J. Donaldson
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Daniel N. Cox
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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  • For correspondence: dcox18@gsu.edu
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Abstract

Cold temperatures can be fatal to insects, but many species have evolved the ability to cold acclimate, thereby increasing their cold tolerance. While there is a growing body of knowledge concerning the mechanisms underlying cold tolerance, relatively little is known concerning how insects sense noxious cold (cold nociception), or how cold nociception might function in cold tolerance. It has been previously shown that Drosophila melanogaster larvae perform highly stereotyped, cold-evoked behaviors under the control of noxious cold-sensing neurons (nociceptors) innervating the barrier epidermis. In the present study, we first sought to describe cold-nociceptive behavior among 11 drosophilid species with differing cold tolerances and from differing climates. Behavioral analyses revealed that the predominant cold-evoked response among drosophilid larvae is a head-to-tail contraction (CT) behavior, which is likely inherited from a common ancestor. However, despite lack of phylogenetic signal (suggesting trait lability), the CT behavior was transient and there was no clear evidence that cold sensitivity was related to thermal environment; collectively this suggests that the behavior might not be adaptive. We therefore sought to uncover an alternative way that cold nociception might be protective. Using a combination of cold-shock assays, optogenetics, electrophysiology, and methods to genetically disrupt neural transmission, we demonstrate that cold sensing neurons in Drosophila melanogaster (Class III nociceptors) are sensitized by and critical to cold acclimation. Moreover, we demonstrate that cold acclimation can be optogenetically-evoked, sans cold. Collectively, these findings reveal that cold nociception constitutes a peripheral neural basis for Drosophila larval cold acclimation.

Significance Statement Many insects adapt to cold in response to developmental exposure to cool temperatures. While there is a growing body of knowledge concerning the mechanisms underlying cold tolerance, it is unknown how sensory neurons might contribute. Here, we show that noxious cold sensing (cold nociception) is widely present among drosophilid larvae, and that cold-sensing neurons (Class III cold nociceptors) are necessary and sufficient drivers of cold acclimation. This suggests that cold acclimation has, at least in part, a neural basis.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 05, 2021.
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The evolution of cold nociception in drosophilid larvae and identification of a neural basis for cold acclimation
Nathaniel J. Himmel, Jamin M. Letcher, Akira Sakurai, Thomas R. Gray, Maggie N. Benson, Kevin J. Donaldson, Daniel N. Cox
bioRxiv 2021.01.04.425280; doi: https://doi.org/10.1101/2021.01.04.425280
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The evolution of cold nociception in drosophilid larvae and identification of a neural basis for cold acclimation
Nathaniel J. Himmel, Jamin M. Letcher, Akira Sakurai, Thomas R. Gray, Maggie N. Benson, Kevin J. Donaldson, Daniel N. Cox
bioRxiv 2021.01.04.425280; doi: https://doi.org/10.1101/2021.01.04.425280

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