Female reproductive fluids ‘rescue’ sperm from phenotypic ageing in an external fertilizer

Abstract

Female reproductive fluids (FRFs) serve key reproductive functions in sexually reproducing animals, including modifying the way sperm swim and detect eggs, and influencing sperm lifespan. Despite the central role of FRF during fertilization, we know surprisingly little about sperm–FRF interactions under different environmental conditions. Theory suggests that in external fertilizers FRF may ‘rescue’ sperm from ageing effects as they search to fertilize eggs. Here, we test the interaction between these two fundamental properties of the fertilization environment, ejaculate age (i.e. time since ejaculation) and FRF, on a range of functional sperm phenotypes in a broadcast spawning mussel, Mytilus galloprovincialis . We found that the effects of ejaculate age on multivariate sperm motility traits and total sperm motility were altered by FRF, and that longer-lived sperm exhibit stronger, likely more advantageous, responses to FRF after periods of ageing. We also detected significant among-male variation in the relationship between sperm motility traits and ejaculate age; notably, these patterns were only revealed when sperm encountered FRF. Collectively these findings underscore the importance of considering female reproductive physiology when interpreting ageing-related declines in sperm motility, as doing so may expose importance sources of variation in sperm phenotypic plasticity among males and environments.

Paternal environment effects are driven by female reproductive fluid but not sperm age in an external fertilizer

“…Fertilization rates were lower in FRF-exposed treatments than in seawater-only treatments, although the effect is small and only manifested for fresh sperm. This finding was unexpected, given fitness-related sperm traits are typically improved by FRF, both in M. galloprovincialis [33,34] and many other taxa [26,28,29]. One possible explanation for this finding is that rapid energy loss resulting from sperm hyperactivation led to overall lower fertilization in our FRF treatment (e.g.…”

“…[14]). In support of this, sperm motility in M. galloprovincialis declines at a faster rate upon exposure to FRF than seawater only [33]. A study of two broadcast spawning invertebrates also attributed fertilization declines to waning sperm energy reserves after sperm incubation in FRF [14].…”

“…Our study uses a powerful within-ejaculate design and the broadcast spawning blue mussel, Mytilus galloprovincialis, a system in which gamete-mediated parental effects have recently been reported [30,31]. We use established methods to manipulate the presence of egg-derived FRF during fertilization [30,32], and exploit dilution effects on sperm metabolism to experimentally age sperm through controlled dilutions [33]. In M. galloprovincialis, FRF typically improves sperm motility (e.g.…”

“…In M. galloprovincialis, FRF typically improves sperm motility (e.g. [33,34]) and ultimately influences fertilization success [34][35][36] and offspring viability [30,34], though the effect of FRF on fertilization and offspring viability depends on the identity of the sperm, egg, and FRF donors [30,34]. With this system, we ask if post-ejaculatory sperm age reduces (i) fertilization success and (ii) offspring survival, and we test the hypothesis that female reproductive fluids can alleviate potential fitness reductions, e.g.…”

Per capita sperm metabolism is density dependent

“…Additionally, a range of studies suggest that dilution in female reproductive fluid (i.e. egg secretions or ovarian fluid) can enhance whole-ejaculate sperm metabolism ( Gray, 1928b ; Hathaway, 1963 ; Ohtake, 1976 ), motility ( Cornman, 1941 ; Gasparini et al, 2020 ; Hadlow et al, 2023 ; Lillie, 1913 ; Poli et al, 2019 ) and longevity ( Gasparini et al, 2020 ; Hadlow et al, 2023 ; Poli et al, 2019 ). Whether this reproductive fluid effect is (1) driven by an enhanced resource uptake following dilution, (2) from an adaptive response to egg cues (i.e.…”