Indirect sexual selection drives rapid sperm protein evolution in abalone

Abstract
Data availability
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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

(2019) NMR assignments for H rufescens FITZAP 8D
Biological Magnetic Resonance Data Bank, 27962.

http://www.bmrb.wisc.edu
(2019) Sequencing of abalone sp18
Genbank, MN102340-MN102343.

https://www.ncbi.nlm.nih.gov/genbank/

The following previously published data sets were used

(1990) Species-specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope
Genbank, M34388, M59969-M59972.

https://www.ncbi.nlm.nih.gov/genbank/
1. Lee YH
2. OtaT
3. Vacquier VD
(1995) Positive selection is a general phenomenon in the evolution of abalone sperm lysin
Genbank, M98875.

https://www.ncbi.nlm.nih.gov/genbank/
(2002) Full-length sequence of VERL, the egg vitelline envelope receptor for abalone sperm lysin
Genbank, AF453553.

https://www.ncbi.nlm.nih.gov/genbank/
(2003) Positive selection in the egg receptor for abalone sperm lysin
Genbank, AF490761-AF490763, AF490765, AF490766.

https://www.ncbi.nlm.nih.gov/genbank/
1. Swanson WJ
2. Vacquier VD
(1995) Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa
Genbank,L36552, L36554, L36589.

https://www.ncbi.nlm.nih.gov/genbank/
1. Palmer MR
2. McDowall MH
3. Stewart L
4. Ouaddi A
5. Maccoss MJ
6. Swanson W
(2013) Mass spectrometry and next-generation sequencing reveal an abundant and rapidly evolving abalone sperm protein
Genbank, AGJ90053, AGJ90054, AGJ90056-AGJ90061.

https://www.ncbi.nlm.nih.gov/genbank/
(2018) Red abalone lysin F104A
BMRB, 30246.

http://www.bmrb.wisc.edu/data_library/summary/index.php?bmrbId=30246

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0002-1255-9982
Lisa M Tuttle

Department of Biochemistry, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8889-232X
Rachel E Klevit

Department of Biochemistry, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3476-969X
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.

Copyright

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.