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- PublicationAccès libreOxidative stress in sperm competition games: experimental tests of the soma vs. germline allocation trade-off in wild house sparrows "Passer domesticus"Female promiscuity leads to the situation where ejaculates of two or more males compete for the fertilization of the ova. Therefore, the reproductive success of a male largely depends on its ejaculate quality, and thus sperm competition exerts strong selection into traits that maximize the fertilizing ability of an ejaculate. Theory predicts that males should progressively increase resource investment into the production of high quality ejaculates as they incur in higher costs to obtain a mate. Yet, the resources being strategically allocated between somatic vs. germline functions remained to be uncovered. Sperm cells are highly vulnerable to oxidative stress (OS), which is known to impair male fertility. Thus, males being able to better protect their ejaculates from oxidative damage should produce higher quality ejaculates. In species where social dominance determines access to fertile females, the oxidation-based soma vs. germline trade-off predicts that subordinate males would strategically allocate more antioxidant resources into their germline, and thus far best in ejaculate quality. In contrast, dominant males should prioritize the protection of their soma over their germline, and thus produce more oxidized and lower quality ejaculates. I tested these predictions using wild House Sparrows Passer domesticus, a passerine species where male reproductive behaviors are associated to their social dominance. To approach the oxidation-based soma vs. germline predictions I experimentally (1) manipulated males’ social status, (2) increased the amount of oxidative stress, and (3) induced an immune response. For those experiments, I explored how male phenotype (e.g. badge and/or dominance) would correlate to germline traits (e.g. sperm morphology, swimming ability) and to patterns of antioxidant allocation into sperm. I found evidence that males that better protect their ejaculates from oxidative damage produced better quality ejaculates, and thus dominant males produced more oxidized and less motile ejaculates (Chapter 1). For instance, when males face higher levels of oxidative stress, they produce ejaculates that are more oxidized and swim at lower speeds (Chapter 5). Differences in ejaculate quality were not explained by differences in sperm morphology, yet the correlations between sperm morphological design and function across social ranks suggest that ejaculate quality depends on the energetics of the sperm cell (Chapter 2). Further, dominant males also produced ejaculates that have larger morphological variation, suggesting that they invest fewer resources into controlling their ejaculate production (Chapter 3). Remarkably, I showed that males can adjust their ejaculate quality and sperm morphological variation to rapid changes of their social environment (Chapters 1 and 3), and that changes in ejaculate quality are paralleled by changes in antioxidant allocation into the ejaculate (Chapter 3). Further, we did not find evidence that male secondary traits would reflect male fertility, yet it seems to signal the oxidative balance of sperm (Chapter 4). Finally, we observed that males at the lower end of the hierarchy could produce ejaculates similar to those of the dominant males, namely their ejaculates had high levels of morphological variation, high oxidative stress, and low motility (Chapters 1 and 3). We suggest that males at the bottom of the hierarchy cannot invest as much resources as predicted into ejaculate quality without compromising their somatic condition. Thus, when they gain positions within a social hierarchy they proportionally increase ejaculate investment (Chapter 1), and they their ejaculates are the most damaged when males face an oxidative challenge (Chapter 5). Altogether, I suggest that under sperm competition oxidative stress and antioxidant allocation are the physiological mechanism modulating male reproductive tactics.
- PublicationAccès libreAntioxidant allocation modulates sperm quality across changing social environmentsIn 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.
- PublicationAccès libreSocial dominance explains within-ejaculate variation in sperm design in a passerine birdComparative studies suggest that sperm competition exerts stabilizing selection towards an optimal sperm design – e.g., the relative size and covariation of different sperm sections or a quantitative measure of sperm shape - that maximizes male fertility, which results in reduced levels of within-male variation in sperm morphology. Yet, these studies also reveal substantial amounts of unexplained within-ejaculate variance, and the factors presiding to the maintenance of such within-male variation in sperm design at the population level still remain to be identified. Sperm competition models predict that males should progressively invest more resources in their germline as their mating costs increase, i.e., the soma/germline allocation trade-off hypothesis. When access to fertile females is determined by social dominance, the soma/germline allocation trade-off hypothesis predicts that dominant males should invest less in the control of spermatogenesis. Hence, dominance should positively correlate with within-male variance in sperm design.
- PublicationAccès libreOxidative stress affects sperm performance and ejaculate redox status in subordinate house sparrowsOxidative stress (OS) is the result of random cellular damage caused by reactive oxygen species that leads to cell death, ageing, or illness. Most physiological processes can result in OS, which in turn has been identified as a major cause of infertility. In promiscuous species, the fertilizing ability of the ejaculate partly determines the male reproductive success. When dominance determines access to fertile females, theory predicts that lower ranking males should increase resource investment into enhancing ejaculate quality. We hypothesized that subordinate males should thus prioritize antioxidant protection of their ejaculates to protect them from OS. We put this hypothesis to the test, by chronically dosing wild House Sparrows with diquat (∼1mg/kg), an herbicide that increases pro-oxidant generation. We found that, although they increased their antioxidant levels in the ejaculate, diquat-treated males produced sperm with reduced velocity. Importantly, and contrary to our hypothesis, males at the bottom of the hierarchy suffered the largest reduction in sperm velocity. We suggest that resource access hinders individuals' ability to cope with environmental hazards. Our results point at OS as a likely physiological mechanism mediating ejaculate quality, while individual ability to access resources may play a role in constraining the extent to which such resources can be allocated into the ejaculate.
- PublicationAccès libreBadge Size Reflects Sperm Oxidative Status within Social Groups in the House Sparrow Passer domesticusThe phenotype-linked fertility hypothesis proposes that male ornaments reflect male fertility. Male ornaments could honestly signal sperm quality due to the high susceptibility of sperm to free radicals on the one hand and the negative impact of oxidative stress on ornament elaboration on the other hand. Thus, only males with superior antioxidant defences could bear the cost of more elaborated sexual ornaments without suffering adverse fitness costs. Yet, in species where males experience differential access to fertile females, a trade-off emerges between investing into traits favouring mating opportunities (e.g. secondary sexual ornaments, social dominance, mate-guarding behaviours, etc.) or into traits favouring sperm competitive ability (e.g. sperm numbers and quality). When male sexual ornaments promote greater access to fertile females, a negative relationship can then be predicted between ornamentation and sperm quality. We tested the latter hypothesis and the phenotype-linked fertility hypothesis in wild House Sparrows Passer domesticus by exploring the relationships between sperm quality, melanin-based ornamentation, and redox status in blood and sperm. We found no correlation between badge size and sperm swimming performance. However, we found that within a social group, large-badged males better protect their ejaculates from oxidative stress, and thus produce less oxidized ejaculates. Additionally, we found that badge size did not reflect social dominance, and thus the protection of the ejaculate is independent of males’ ability to monopolize resources. Our results suggest that badge size might reflect male investment into the antioxidant protection of their sperm relative to a given social environment, and thus females may accrue both direct and indirect benefits by mating with large-badged males producing less oxidized ejaculates.