Unique transcriptional signatures of sleep loss across independently evolved cavefish populations

Suzanne E. McGaugh, Courtney N. Passow, James Brian Jaggard, Bethany A. Stahl, Alex C. Keene

Research output: Contribution to journalArticlepeer-review

Abstract

Animals respond to sleep loss with compensatory rebound sleep, and this is thought to be critical for the maintenance of physiological homeostasis. Sleep duration varies dramatically across animal species, but it is not known whether evolutionary differences in sleep duration are associated with differences in sleep homeostasis. The Mexican cavefish, Astyanax mexicanus, has emerged as a powerful model for studying the evolution of sleep. While eyed surface populations of A. mexicanus sleep approximately 8 hr each day, multiple blind cavefish populations have converged on sleep patterns that total as little as 2 hr each day, providing the opportunity to examine whether the evolution of sleep loss is accompanied by changes in sleep homeostasis. Here, we examine the behavioral and molecular response to sleep deprivation across four independent populations of A. mexicanus. Our behavioral analysis indicates that surface fish and all three cavefish populations display robust recovery sleep during the day following nighttime sleep deprivation, suggesting sleep homeostasis remains intact in cavefish. We profiled transcriptome-wide changes associated with sleep deprivation in surface fish and cavefish. While the total number of differentially expressed genes was not greater for the surface population, the surface population exhibited the highest number of uniquely differentially expressed genes than any other population. Strikingly, a majority of the differentially expressed genes are unique to individual cave populations, suggesting unique expression responses are exhibited across independently evolved cavefish populations. Together, these findings suggest sleep homeostasis is intact in cavefish despite a dramatic reduction in overall sleep duration.

Original languageEnglish (US)
Pages (from-to)497-510
Number of pages14
JournalJournal of Experimental Zoology Part B: Molecular and Developmental Evolution
Volume334
Issue number7-8
DOIs
StatePublished - Nov 1 2020

Bibliographical note

Funding Information:
We thank the University of Minnesota Genomics Center for their guidance and performing the cDNA library preparations and Illumina HiSeq 2500 sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this paper. Funding was supported by NIH (1R01GM127872-01 to S. E. M. and A. C. K.) and NSF award IOS 165674 to A. C. K., and a US-Israel BSF award to A.C.K. C.N.P. was supported by Grand Challenges in Biology Postdoctoral Program at the University of Minnesota College of Biological Sciences. Institutional Animal Care and Use Committee at Florida Atlantic University (Protocol #A15-32).

Funding Information:
We thank the University of Minnesota Genomics Center for their guidance and performing the cDNA library preparations and Illumina HiSeq 2500 sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this paper. Funding was supported by NIH (1R01GM127872‐01 to S. E. M. and A. C. K.) and NSF award IOS 165674 to A. C. K., and a US‐Israel BSF award to A.C.K. C.N.P. was supported by Grand Challenges in Biology Postdoctoral Program at the University of Minnesota College of Biological Sciences. Institutional Animal Care and Use Committee at Florida Atlantic University (Protocol #A15‐32).

Publisher Copyright:
© 2020 Wiley Periodicals, Inc.

Keywords

  • Astyanax mexicanus
  • RNAseq
  • convergent evolution
  • sleep homeostasis

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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