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Research Article
Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex
Kimberly S. Sheldon, Mojgan Padash, Amanda W. Carter, Katie E. Marshall
Journal of Experimental Biology 2020 223: jeb233239 doi: 10.1242/jeb.233239 Published 9 December 2020
Kimberly S. Sheldon
1Department of Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN 37996, USA
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  • ORCID record for Kimberly S. Sheldon
  • For correspondence: ksheldon@utk.edu
Mojgan Padash
2Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
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Amanda W. Carter
1Department of Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN 37996, USA
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Katie E. Marshall
3Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, BC, Canada V6T 1Z4
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ABSTRACT

Most studies exploring molecular and physiological responses to temperature have focused on constant temperature treatments. To gain a better understanding of the impact of fluctuating temperatures, we investigated the effects of increased temperature variation on Phanaeus vindex dung beetles across levels of biological organization. Specifically, we hypothesized that increased temperature variation is energetically demanding. We predicted that thermal sensitivity of metabolic rate and energetic reserves would be reduced with increasing fluctuation. To test this, we examined the responses of dung beetles to constant (20°C), low fluctuation (20±5°C), or high fluctuation (20±12°C) temperature treatments using respirometry, assessment of energetic reserves and HPLC-MS-based metabolomics. We found no significant differences in metabolic rate or energetic reserves, suggesting increased fluctuations were not energetically demanding. To understand why there was no effect of increased amplitude of temperature fluctuation on energetics, we assembled and annotated a de novo transcriptome, finding non-overlapping transcriptomic and metabolomic responses of beetles exposed to different fluctuations. We found that 58 metabolites increased in abundance in both fluctuation treatments, but 15 only did so in response to high-amplitude fluctuations. We found that 120 transcripts were significantly upregulated following acclimation to any fluctuation, but 174 were upregulated only in beetles from the high-amplitude fluctuation treatment. Several differentially expressed transcripts were associated with post-translational modifications to histones that support a more open chromatin structure. Our results demonstrate that acclimation to different temperature fluctuations is distinct and may be supported by increasing transcriptional plasticity. Our results indicate for the first time that histone modifications may underlie rapid acclimation to temperature variation.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: K.S.S., K.E.M.; Methodology: K.S.S., M.P., K.E.M.; Validation: K.S.S., K.E.M.; Formal analysis: K.S.S., A.W.C., K.E.M.; Investigation: K.S.S., M.P., K.E.M.; Resources: K.S.S., K.E.M.; Data curation: K.S.S., K.E.M.; Writing - original draft: K.S.S., K.E.M., A.W.C.; Writing - review & editing: K.S.S., M.P., A.W.C., K.E.M.; Visualization: K.S.S., A.W.C., K.E.M.; Supervision: K.S.S., K.E.M.; Project administration: K.S.S., K.E.M.; Funding acquisition: K.S.S., K.E.M.

  • Funding

    This research was supported by the US National Science Foundation Division of Integrative Organismal Systems [IOS-1930829 to K.S.S. and K.E.M.].

  • Data availability

    Raw metabolomics data, metabolic rate data, and carbohydrate and lipid data are available from Open Science Framework (doi:10.17605/OSF.IO/H34J2, https://osf.io/h34j2/). Raw transcriptomic read data have been archived in the NCBI database under Bioproject accession PRJNA667000.

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.233239.supplemental

  • Received July 15, 2020.
  • Accepted October 27, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Coleoptera
  • Histones
  • Insects
  • Metabolism
  • Temperature variation
  • Thermal physiology

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Research Article
Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex
Kimberly S. Sheldon, Mojgan Padash, Amanda W. Carter, Katie E. Marshall
Journal of Experimental Biology 2020 223: jeb233239 doi: 10.1242/jeb.233239 Published 9 December 2020
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Research Article
Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex
Kimberly S. Sheldon, Mojgan Padash, Amanda W. Carter, Katie E. Marshall
Journal of Experimental Biology 2020 223: jeb233239 doi: 10.1242/jeb.233239 Published 9 December 2020

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