Abstract
In promiscuous species, male reproductive success depends on their ability to mate with fertile females and on the fertilizing ability of their sperm. In such species, theory predicts that, owing to a trade-off between pre- and post-copulatory reproductive traits, males with lesser access to females should increase resource investment into those sperm traits that enhance fertilization success–usually referred to as ejaculate quality. This prediction has been validated in several taxa, yet studies on the physiological mechanisms modulating ejaculate quality are lacking. Sperm cells are highly vulnerable to oxidative stress, which impairs male fertility. Therefore, males that better protect their sperm from oxidative stress are expected to achieve higher ejaculate quality. Based on theoretical expectations, and since social dominance is a major determinant of mating opportunity, we predicted that subordinate males should invest more into the antioxidant protection of their sperm in order to achieve higher ejaculate quality. We maintained 60 male and 60 female wild-caught house sparrows Passer domesticus in outdoor aviaries, where we experimentally manipulated male social status to test our predictions. We measured cellular oxidative stress and enzymatic antioxidant activity in blood and sperm both before and after manipulating social ranks. Before manipulating the social status, we found that ejaculate viability correlated with oxidative stress level in sperm, with dominant males producing more oxidized and less viable ejaculates. Further, males at the lower end of the hierarchy produced ejaculates of similar quality to those of dominant males, suggesting that restricted access to resources might limit male reproductive strategies. After experimentally manipulating the social status, males matched their ejaculate quality to their new rank, while increases in antioxidant investment into ejaculates paralleled increases in ejaculate viability. Oxidative stress has been proposed as a general constraint to the evolution of life histories. Our results highlight oxidative stress and strategic antioxidant allocation as important proximate physiological mechanisms underlying male reproductive strategies.
Highlights
Antioxidant allocation, sperm quality and social status. Sexual selection arises both before copulation because males differ in their ability to access fertile females, and after copulation inside the female reproductive tract when the sperm of two or more males compete to fertilize the ova, a circumstance referred to as sperm competition [1]
We found that ejaculates produced by males with different social ranks differed in their initial viability (% of motile sperm) (Fig 1A; Table 1), with subordinate males 1 and 2 producing more viable ejaculates than dominant and subordinate 3 males
We found that the proportion of oxidized over total concentration of glutathione in the ejaculate varied according to the social status (Fig 1; social status: F3,48 = 2.96, p = 0.04; body mass: F48.5 < 0.01, p = 0.98; tarsus length: F48.1 = 0.63, p = 0.43), with dominant and subordinate 3 males having more oxidatively stressed sperm cells
Summary
Sexual selection arises both before copulation because males differ in their ability to access fertile females, and after copulation inside the female reproductive tract when the sperm of two or more males compete to fertilize the ova, a circumstance referred to as sperm competition [1]. Selection acts upon those ejaculate traits (e.g. sperm velocity, proportion of motile sperm, ATP production, etc.; generally referred to as ejaculate quality) that maximize fertilization success (reviewed in [4, 5, 6]). Several theoretical models have explored how much males are selected to invest into post-copulatory traits, i.e. ejaculate quality and competitiveness, given variation in their ability to mate with fertile females (reviewed in [3, 7]). These models predict a negative correlation between ejaculate quality and social dominance. Several studies have investigated the potential outcomes of a soma vs. germline allocation trade-off, the actual resources to be strategically allocated to the germline are yet to be identified
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