Indirect sexual selection drives rapid sperm protein evolution in abalone
- University of Washington, United States
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.
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NMR assignments for H rufescens FITZAP 8DBiological Magnetic Resonance Data Bank, 27962.
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Positive selection in the egg receptor for abalone sperm lysinGenbank, AF490761-AF490763, AF490765, AF490766.
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Mass spectrometry and next-generation sequencing reveal an abundant and rapidly evolving abalone sperm proteinGenbank, AGJ90053, AGJ90054, AGJ90056-AGJ90061.
Article and author information
Author details
Damien Beau Wilburn
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
- Hannes Neuweiler, University of Würzburg, Germany
Version history
- Received: October 10, 2019
- Accepted: December 20, 2019
- Accepted Manuscript published: December 23, 2019 (version 1)
- 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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Indirect sexual selection drives rapid sperm protein evolution in abalone
eLife 8:e52628.
https://doi.org/10.7554/eLife.52628
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