1. Evolutionary Biology
  2. Structural Biology and Molecular Biophysics

Indirect sexual selection drives rapid sperm protein evolution in abalone

  1. Damien Beau Wilburn  Is a corresponding author
  2. Lisa M Tuttle
  3. Rachel E Klevit
  4. Willie J Swanson
  1. University of Washington, United States
https://doi.org/10.7554/eLife.52628
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  1. Damien Beau Wilburn
  2. Lisa M Tuttle
  3. Rachel E Klevit
  4. Willie J Swanson
(2019)
Indirect sexual selection drives rapid sperm protein evolution in abalone
eLife 8:e52628.
https://doi.org/10.7554/eLife.52628
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Abstract

Sexual selection can explain the rapid evolution of fertilization proteins, yet sperm proteins evolve rapidly even if not directly involved in fertilization. In the marine mollusk abalone, sperm secrete enormous quantities of two rapidly evolving proteins, lysin and sp18, that are stored at nearly molar concentrations. We demonstrate that this extraordinary packaging is achieved by associating into Fuzzy Interacting Transient Zwitterion (FITZ) complexes upon binding the intrinsically disordered FITZ Anionic Partner (FITZAP). FITZ complexes form at intracellular ionic strengths, and upon exocytosis into seawater, lysin and sp18 are dispersed to drive fertilization. NMR analyses revealed that lysin uses a common molecular interface to bind both FITZAP and its egg receptor VERL. As sexual selection alters the lysin-VERL interface, FITZAP coevolves rapidly to maintain lysin binding. FITZAP-lysin interactions exhibit a similar species-specificity as lysin-VERL interactions. Thus, tethered molecular arms races driven by sexual selection can generally explain rapid sperm protein evolution.

Data availability

Sequences have been deposited into Genbank under Accession # MN102340-MN102343 and NMR data have been deposited in the BMRB under accession code 27962.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Damien Beau Wilburn

    Department of Genome Sciences, University of Washington, Seattle, United States
    For correspondence
    dwilburn@u.washington.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1255-9982

  2. Lisa M Tuttle

    Department of Biochemistry, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8889-232X

  3. Rachel E Klevit

    Department of Biochemistry, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3476-969X

  4. Willie J Swanson

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01-HD076862)

  • Willie J Swanson

Eunice Kennedy Shriver National Institute of Child Health and Human Development (K99-HD090201)

  • Damien Beau Wilburn

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

Reviewing Editor

  1. Hannes Neuweiler, University of Würzburg, Germany

Publication history

  1. Received: October 10, 2019
  2. Accepted: December 20, 2019
  3. Accepted Manuscript published: December 23, 2019 (version 1)
  4. Version of Record published: January 9, 2020 (version 2)

Copyright

© 2019, Wilburn 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. Damien Beau Wilburn
  2. Lisa M Tuttle
  3. Rachel E Klevit
  4. Willie J Swanson
(2019)
Indirect sexual selection drives rapid sperm protein evolution in abalone
eLife 8:e52628.
https://doi.org/10.7554/eLife.52628

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