Multifactorial processes underlie parallel opsin loss in neotropical bats

  1. Alexa Sadier
  2. Kalina TJ Davies
  3. Laurel R Yohe
  4. Kun Yun
  5. Paul Donat
  6. Brandon P Hedrick
  7. Elizabeth R Dumont
  8. Liliana M Dávalos  Is a corresponding author
  9. Stephen J Rossiter  Is a corresponding author
  10. Karen E Sears  Is a corresponding author
  1. University of California, Los Angeles, United States
  2. Queen Mary University of London, United Kingdom
  3. Stony Brook University, United States
  4. University of Illinois, United States
  5. Harvard University, United States
  6. University of California, Merced, United States

Abstract

The loss of previously adaptive traits is typically linked to relaxation in selection, yet the molecular steps leading to such repeated losses are rarely known. Molecular studies of loss have tended to focus on gene sequences alone, but overlooking other aspects of protein expression might underestimate phenotypic diversity. Insights based almost solely on opsin gene evolution, for instance, have made mammalian color vision a textbook example of phenotypic loss. We address this gap by investigating retention and loss of opsin genes, transcripts and proteins across ecologically diverse noctilionoid bats. We find multiple, independent losses of short-wave sensitive opsins. Mismatches between putatively functional DNA sequences, mRNA transcripts, and proteins implicate transcriptional and post-transcriptional processes in the ongoing loss of S-opsins in some noctilionoid bats. Our results provide a snapshot of evolution in progress during phenotypic trait loss, and suggest vertebrate visual phenotypes cannot always be predicted from genotypes alone.

Data availability

Sequencing data have been deposited in GenBank in the Nucleotide Database. The accession numbers are as follows: RHO: MK209460 - MK209505; OPN1LW: MK209506 - MK209551; OPN1SW: MK209552 - MK209592. The GenBank numbers for the OPN1SW PCR sequences are MK248618 - MK248630. Gene alignments are available via Dryad (http://dx.doi.org/10.5061/dryad.456569k).

The following data sets were generated

Article and author information

Author details

  1. Alexa Sadier

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9907-3714
  2. Kalina TJ Davies

    School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Laurel R Yohe

    Department of Ecology and Evolution, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1567-8749
  4. Kun Yun

    Department of Animal Biology, University of Illinois, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Paul Donat

    Department of Ecology and Evolution, Stony Brook University, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Brandon P Hedrick

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4446-3405
  7. Elizabeth R Dumont

    School of Natural Sciences, University of California, Merced, Merced, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Liliana M Dávalos

    Department of Ecology and Evolution, Stony Brook University, Stony Brook, United States
    For correspondence
    liliana.davalos-alvarez@stonybrook.edu
    Competing interests
    The authors declare that no competing interests exist.
  9. Stephen J Rossiter

    School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    For correspondence
    s.j.rossiter@qmul.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  10. Karen E Sears

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    ksears@ucla.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9744-9602

Funding

National Science Foundation (1442142)

  • Kalina TJ Davies
  • Laurel R Yohe
  • Stephen J Rossiter

National Science Foundation (1442314)

  • Alexa Sadier
  • Kun Yun
  • Karen E Sears

National Science Foundation (1442278)

  • Paul Donat
  • Brandon P Hedrick
  • Elizabeth R Dumont

European Research Council (310482)

  • Kalina TJ Davies
  • Stephen J Rossiter

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols 14199 at UIUC and 2017-093 at UCLA. Every effort was made to minimize suffering.

Copyright

© 2018, Sadier et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alexa Sadier
  2. Kalina TJ Davies
  3. Laurel R Yohe
  4. Kun Yun
  5. Paul Donat
  6. Brandon P Hedrick
  7. Elizabeth R Dumont
  8. Liliana M Dávalos
  9. Stephen J Rossiter
  10. Karen E Sears
(2018)
Multifactorial processes underlie parallel opsin loss in neotropical bats
eLife 7:e37412.
https://doi.org/10.7554/eLife.37412

Share this article

https://doi.org/10.7554/eLife.37412

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