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

Abstract

Post-copulatory sexual selection processes, including sperm competition and cryptic female choice (CFC), can operate based on major histocompatibility (MH) genes. We investigated sperm competition between male alternative reproductive tactics [jack (sneaker) and hooknose (guard)] of Chinook salmon (Oncorhynchus tshawytscha). Using a full factorial design, we examined in vitro competitive fertilization success of paired jack and hooknose males at three time points after sperm activation (0, 15 and 60 s) to test for male competition, CFC and time effects on male fertilization success. We also examined egg-mediated CFC at two MH genes by examining both the relationship between competitive fertilization success and MH divergence as well as inheritance patterns of MH alleles in resulting offspring. We found that jacks sired more offspring than hooknose males at 0 s post-activation; however, jack fertilization success declined over time post-activation, suggesting a trade-off between sperm speed and longevity. Enhanced fertilization success of jacks (presumably via higher sperm quality) may serve to increase sneaker tactic competitiveness relative to dominant hooknose males. We also found evidence of egg-mediated CFC (i.e. female 9 male interaction) influencing competitive fertilization success; however, CFC was not acting on the MH genes as we found no relationship between fertilization success and MH II b 1 or MH I a 1 divergence and we found no deviations from Mendelian inheritance of MH alleles in the offspring. Our study provides insight into evolutionary mechanisms influencing variation in male mating success within alternative reproductive tactics, thus underscoring different strategies that males can adopt to attain success.

No support for cryptic choice by ovarian fluid in an external fertilizer

“…This way of separating eggs and OF, by draining OF from the eggs, is probably similar to the draining of OF as reported by Lehnert et al. (). Thereafter, the OF was returned to the same eggs (i.e., “own OF”).…”

“…The OF, now located at the lower part of the petri dish, was carefully removed with a pipette from the lowest point of the petri dish. This way of separating eggs and OF, by draining OF from the eggs, is probably similar to the draining of OF as reported by Lehnert et al (2018). Thereafter, the OF was returned to the same eggs (i.e., "own OF").…”

“…The inconsistency between studies is currently hard to explain, but may be related to different experimental designs, species‐specific effects, or some other unidentified variable. Additionally, micropylar sperm attractants at the egg surface within and immediately around the narrow micropylar opening leading to the egg interior have been suggested to attract or guide nearby spermatozoa toward and through the micropyle and may thus have the potential to affect sperm selection (Iwamatsu, Yoshizaki, & Shibata, ; Lehnert et al, ; Mengerink & Vacquier, ; Yanagimachi et al, ; Yanagimachi, Cherr, Pillai, & Baldwin, ). In fishes, glycoproteins are examples of such micropylar sperm attractants described (Iwamatsu et al, ; Yanagimachi et al, ).…”

“…Recent reviews and meta-analysis have, however, provided weak evidence for genetic benefits from polyandry (Slatyer, Mautz, Backwell, & Jennions, 2012) and few clear demonstrations of cryptic female choice (Firman et al, 2017). Whereas some studies on external fertilizers have reported increased fertilization success for the male whose sperm swims faster in the females' OF (e. g. Evans, Rosengrave, Gasparini, & Gemmell, 2013;Rosengrave, Montgomerie, & Gemmell, 2016;Lehnert, Butts, et al, 2017;Lehnert, Helou, Pitcher, Heath, & Heath, 2018), another study found no such relationship (Lehnert, Heath, Devlin, & Pitcher, 2017). Additionally, no effect of cryptic female choice on offspring fitness was documented in salmon (Salmo salar) reported by Lumley et al (2016).…”

Exposure to exogenous egg cortisol does not rescue juvenile Chinook salmon body size, condition, or survival from the effects of elevated water temperatures

“…At the aquatic facility, we filled individual containers with 90 g of eggs (~300 eggs) from each of the 15 females and added ~0.5 ml (4 drops) of pooled milt from the nine males. After gently swilling the egg–milt solution we added 60 ml of river water to activate the sperm (Lehnert, Helou, Pitcher, Heath, & Heath, ). After 2 min (when sperm should no longer be motile), we added river water mixed to 1,000 ng/ml concentration of cortisol (H4001; Sigma‐Aldrich Canada Co) dissolved in 90% ethanol (HPLC grade; Sigma‐Aldrich Canada Co) or 0 ng/ml control solution (ethanol and water only) for a 2‐hr incubation.…”