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

Abstract

Gamete-level sexual selection of externally fertilising species is usually achieved by modifying sperm behaviour with mechanisms thought to 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 its biochemical effects 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 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, thus indicating a shear-thickening phase where viscosity increases provided it is probed gently enough. This suggests the presence of a unique frequency-dependant structural network with relevant implications on sperm energetics and fertilisation dynamics.