Ovarian fluid impacts flagellar beating and biomechanical metrics of sperm between alternative reproductive tactics

Abstract

Alternative reproductive tactics (ARTs) are prevalent in nature, where smaller parasitic males typically have better sperm quality than larger territorial guard males. At present, it is unclear what is causing this phenomenon. Our objective was to gain insights into sperm form and function by examining flagellar beating patterns (beat frequency, wave amplitude, bend length, bend angle, wave velocity) and biomechanical sperm metrics (velocity, hydrodynamic power output, propulsive efficiency) of wild spawning Chinook salmon ARTs. Ovarian fluid and milt were collected to form a series of eight experimental blocks, each composed of ovarian fluid from a unique female and sperm from a unique pair of parasitic jack and guard hooknose males. Sperm from each ART were activated in river water and ovarian fluid. Flagellar parameters were evaluated from recordings using high-speed video microscopy and biomechanical metrics were quantified. We show that ART has an impact on flagellar beating, where jacks had a higher bend length and bend angle than hooknoses. Activation media also impacted the pattern of flagellar parameters, such that beat frequency, wave velocity and bend angle declined, while wave amplitude of flagella increased when ovarian fluid was incorporated into activation media. Furthermore, we found that sperm from jacks swam faster than those from hooknoses and required less hydrodynamic power output to propel themselves in river water and ovarian fluid. Jack sperm were also more efficient at swimming than hooknose sperm, and propulsive efficiency increased when cells were activated in ovarian fluid. The results demonstrate that sperm biomechanics may be driving divergence in competitive reproductive success between ARTs.

Assessing the potential for post‐ejaculatory female choice in a polyandrous beach‐spawning fish

“…We therefore expected to find post‐ejaculation selection in the form of cryptic female choice mediated by egg cues in capelin. However, we found no evidence that egg water influences sperm swimming characteristics in relation to its concentration (dose) or as a consequence of female–male identity interaction, despite contrary findings in other fishes (Butts, Prokopchuk, Kašpar, Cosson, & Pitcher, ; Elofsson et al, ; Lahnsteiner, ; Lehnert, Butts, et al, ; Lehnert, Devlin, et al, ; Litvak & Trippel, ; Poli et al, ; Rosengrave et al, ; Turner & Montgomerie, ; Urbach et al, ; Yeates et al, ). As capelin often spawn on the beach in threesomes, sperm competition risk (probability of competition with one other male; Parker, Ball, Stockley, & Gage, ) is likely to be high, but intensity (the number of competing males; Parker, Ball, Stockley, & Gage, ) will be low.…”

Sperm competition, but not major histocompatibility divergence, drives differential fertilization success between alternative reproductive tactics in Chinook salmon

“…We found no significant effect of female identity on competitive fertilization success; however, we did find a significant female 9 sire-pair interaction effect indicating evidence of cryptic female choice (CFC). In salmonids, CFC may be mediated by the egg and/or ovarian fluid characteristics (Lahnsteiner, 2002;Rosengrave et al, 2009Rosengrave et al, , 2016Yeates et al, 2009Yeates et al, , 2014Butts et al, 2012bButts et al, , 2017Gessner et al, 2017a, b). Although ovarian fluid can influence the outcome of sperm competition between jack and hooknose males (see Butts et al, 2017;Lehnert et al, 2017), ovarian fluid was removed from the eggs in our study and therefore evidence of CFC may only be explained by egg-sperm interactions.…”

“…Given that there is evidence for a strong additive genetic component to jacking rates (Heath et al, 1994), one would expect that selection for jacks would occur over a relatively short period of time under hatchery conditions. Therefore, hatcheries should attempt to mimic natural spawning, and one way in which hatcheries could provide more natural conditions during fertilization would be by including ovarian fluid in fertilization protocols, as ovarian fluid has been reported to allow both tactics to attain similar success during in vitro competitive fertilization (Butts et al, 2017;Lehnert et al, 2017). Hatcheries play a crucial role in the management and conservation of salmon; therefore, it is of great importance that more genetically benign management strategies are implemented (Campton, 2005).…”

Post‐ejaculatory modifications to sperm (PEMS)

“…Similarly, two kinds of studies implicate a role for ovarian fluid in mediating sexual selection within populations. First, ovarian fluid has been shown to affect differentially the behaviour of sperm from males exhibiting alternative reproductive tactics (Alonzo, Stiver, & Marsh-Rollo, 2016;Butts et al, 2017;Lehnert et al, 2017aLehnert et al, , 2017b. Second, the chemical composition of ovarian fluid differs among females within populations (Rosengrave et al, 2008;Johnson et al, 2014), with the influence of ovarian fluid on sperm behaviour being significantly influenced by female identity, male identity and female × male interaction (Rosengrave et al, 2008).…”