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Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages

View ORCID ProfilePhilip J. Freda, View ORCID ProfileJantina Toxopeus, Edwina J. Dowle, Zainab M. Ali, Nicholas Heter, Rebekah L. Lambert-Collier, Isaiah Sower, Joseph C. Tucker, View ORCID ProfileTheodore J. Morgan, View ORCID ProfileGregory J. Ragland
doi: https://doi.org/10.1101/2022.01.16.476527
Philip J. Freda
1Department of Entomology, Kansas State University, 1603 Old Claflin Place, Manhattan, KS 66506, U.S.A.
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  • For correspondence: philip.freda@gmail.com philip.freda@cshs.org
Jantina Toxopeus
2Department of Integrative Biology, University of Colorado Denver, 1151 Arapahoe St., Denver, CO 80204, U.S.A.
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Edwina J. Dowle
2Department of Integrative Biology, University of Colorado Denver, 1151 Arapahoe St., Denver, CO 80204, U.S.A.
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Zainab M. Ali
3Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, U.S.A.
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Nicholas Heter
3Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, U.S.A.
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Rebekah L. Lambert-Collier
3Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, U.S.A.
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Isaiah Sower
2Department of Integrative Biology, University of Colorado Denver, 1151 Arapahoe St., Denver, CO 80204, U.S.A.
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Joseph C. Tucker
2Department of Integrative Biology, University of Colorado Denver, 1151 Arapahoe St., Denver, CO 80204, U.S.A.
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Theodore J. Morgan
3Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, U.S.A.
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Gregory J. Ragland
2Department of Integrative Biology, University of Colorado Denver, 1151 Arapahoe St., Denver, CO 80204, U.S.A.
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  • ORCID record for Gregory J. Ragland
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Abstract

Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation (genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved Cellular Stress Response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNAi (RNA interference) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to -5°C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we found no relationship between stage-specificity and tissue-specificity of transcripts, suggesting that the differences are not simply driven by differences in tissue composition across development. In addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages.

Summary Statement RNAseq and gene knockout via transgenic RNAi lines suggest that physiological responses to low temperatures are largely distinct across life stages of the fly Drosophila melanogaster.

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. All rights reserved. No reuse allowed without permission.
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Posted January 19, 2022.
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Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages
Philip J. Freda, Jantina Toxopeus, Edwina J. Dowle, Zainab M. Ali, Nicholas Heter, Rebekah L. Lambert-Collier, Isaiah Sower, Joseph C. Tucker, Theodore J. Morgan, Gregory J. Ragland
bioRxiv 2022.01.16.476527; doi: https://doi.org/10.1101/2022.01.16.476527
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Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages
Philip J. Freda, Jantina Toxopeus, Edwina J. Dowle, Zainab M. Ali, Nicholas Heter, Rebekah L. Lambert-Collier, Isaiah Sower, Joseph C. Tucker, Theodore J. Morgan, Gregory J. Ragland
bioRxiv 2022.01.16.476527; doi: https://doi.org/10.1101/2022.01.16.476527

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