Oxidative 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 <i>Passer domesticus</i>, 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.

Thèse de doctorat : Université de Neuchâtel, 2016