Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions

Gamete-level sexual selection of externally fertilising species is usually achieved by modifying sperm behaviour with mechanisms that alter the chemical environment in which gametes perform. In fish, this can be accomplished through the ovarian fluid, a substance released with the eggs at spawning....

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Published in:Journal of Experimental Biology
Main Authors: Graziano, Marco, Palit, Swomitra, Yethiraj, Anand, Immler, Simone, Gage, Matthew J. G., Purchase, Craig F.
Format: Text
Language:English
Published: The Company of Biologists Ltd 2023
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/
http://www.ncbi.nlm.nih.gov/pubmed/36511132
https://doi.org/10.1242/jeb.244712
id ftpubmed:oai:pubmedcentral.nih.gov:10086386
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10086386 2023-06-06T11:52:02+02:00 Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions Graziano, Marco Palit, Swomitra Yethiraj, Anand Immler, Simone Gage, Matthew J. G. Purchase, Craig F. 2023-01-13 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/ http://www.ncbi.nlm.nih.gov/pubmed/36511132 https://doi.org/10.1242/jeb.244712 en eng The Company of Biologists Ltd http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/ http://www.ncbi.nlm.nih.gov/pubmed/36511132 http://dx.doi.org/10.1242/jeb.244712 © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. J Exp Biol Research Article Text 2023 ftpubmed https://doi.org/10.1242/jeb.244712 2023-04-16T00:53:43Z Gamete-level sexual selection of externally fertilising species is usually achieved by modifying sperm behaviour with mechanisms that alter the chemical environment in which gametes perform. In fish, this can be accomplished through the ovarian fluid, a substance released with the eggs at spawning. While the biochemical effects of ovarian fluid in relation to sperm energetics have been investigated, the influence of the physical environment in which sperm compete remains poorly explored. Our objective was therefore to gain insights on the physical structure of this fluid and potential impacts on reproduction. Using soft-matter physics approaches of steady-state and oscillatory viscosity measurements, we subjected wild Atlantic salmon ovarian fluids to variable shear stresses and frequencies resembling those exerted by sperm swimming through the fluid near eggs. We show that this fluid, which in its relaxed state is a gel-like substance, displays a non-Newtonian viscoelastic and shear-thinning profile, where the viscosity decreases with increasing shear rates. We concurrently find that this fluid obeys the Cox–Merz rule below 7.6 Hz and infringes it above this level, thus indicating a shear-thickening phase where viscosity increases provided it is probed gently enough. This suggests the presence of a unique frequency-dependent structural network with relevant implications for sperm energetics and fertilisation dynamics. This article has an associated ECR Spotlight interview with Marco Graziano. Text Atlantic salmon PubMed Central (PMC) Merz ENVELOPE(-61.061,-61.061,-72.311,-72.311) Journal of Experimental Biology 226 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Graziano, Marco
Palit, Swomitra
Yethiraj, Anand
Immler, Simone
Gage, Matthew J. G.
Purchase, Craig F.
Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
topic_facet Research Article
description Gamete-level sexual selection of externally fertilising species is usually achieved by modifying sperm behaviour with mechanisms that alter the chemical environment in which gametes perform. In fish, this can be accomplished through the ovarian fluid, a substance released with the eggs at spawning. While the biochemical effects of ovarian fluid in relation to sperm energetics have been investigated, the influence of the physical environment in which sperm compete remains poorly explored. Our objective was therefore to gain insights on the physical structure of this fluid and potential impacts on reproduction. Using soft-matter physics approaches of steady-state and oscillatory viscosity measurements, we subjected wild Atlantic salmon ovarian fluids to variable shear stresses and frequencies resembling those exerted by sperm swimming through the fluid near eggs. We show that this fluid, which in its relaxed state is a gel-like substance, displays a non-Newtonian viscoelastic and shear-thinning profile, where the viscosity decreases with increasing shear rates. We concurrently find that this fluid obeys the Cox–Merz rule below 7.6 Hz and infringes it above this level, thus indicating a shear-thickening phase where viscosity increases provided it is probed gently enough. This suggests the presence of a unique frequency-dependent structural network with relevant implications for sperm energetics and fertilisation dynamics. This article has an associated ECR Spotlight interview with Marco Graziano.
format Text
author Graziano, Marco
Palit, Swomitra
Yethiraj, Anand
Immler, Simone
Gage, Matthew J. G.
Purchase, Craig F.
author_facet Graziano, Marco
Palit, Swomitra
Yethiraj, Anand
Immler, Simone
Gage, Matthew J. G.
Purchase, Craig F.
author_sort Graziano, Marco
title Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
title_short Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
title_full Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
title_fullStr Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
title_full_unstemmed Frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
title_sort frequency-dependent viscosity of salmon ovarian fluid has biophysical implications for sperm–egg interactions
publisher The Company of Biologists Ltd
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/
http://www.ncbi.nlm.nih.gov/pubmed/36511132
https://doi.org/10.1242/jeb.244712
long_lat ENVELOPE(-61.061,-61.061,-72.311,-72.311)
geographic Merz
geographic_facet Merz
genre Atlantic salmon
genre_facet Atlantic salmon
op_source J Exp Biol
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/
http://www.ncbi.nlm.nih.gov/pubmed/36511132
http://dx.doi.org/10.1242/jeb.244712
op_rights © 2023. Published by The Company of Biologists Ltd
https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
op_doi https://doi.org/10.1242/jeb.244712
container_title Journal of Experimental Biology
container_volume 226
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