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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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Autores principales: Graziano, Marco, Palit, Swomitra, Yethiraj, Anand, Immler, Simone, Gage, Matthew J. G., Purchase, Craig F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/
https://www.ncbi.nlm.nih.gov/pubmed/36511132
http://dx.doi.org/10.1242/jeb.244712
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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
collection PubMed
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.
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spelling pubmed-100863862023-04-12 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. J Exp Biol Research Article 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. The Company of Biologists Ltd 2023-01-13 /pmc/articles/PMC10086386/ /pubmed/36511132 http://dx.doi.org/10.1242/jeb.244712 Text en © 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.
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
title 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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086386/
https://www.ncbi.nlm.nih.gov/pubmed/36511132
http://dx.doi.org/10.1242/jeb.244712
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