Sperm sex ratio adjustment in a mammal: perceived male competition leads to elevated proportions of female-producing sperm

Sperm sex ratio adjustment in a mammal: perceived male competition leads to elevated proportions of female-producing sperm. Renée C. Firman, Jamie N. Tedeschi and Francisco Garcia-Gonzalez. Biology Letters, June 3 2020. https://doi.org/10.1098/rsbl.2019.0929

Abstract: Mammal sex allocation research has focused almost exclusively on maternal traits, but it is now apparent that fathers can also influence offspring sex ratios. Parents that produce female offspring under conditions of intense male–male competition can benefit with greater assurance of maximized grand-parentage. Adaptive adjustment in the sperm sex ratio, for example with an increase in the production of X-chromosome bearing sperm (CBS), is one potential paternal mechanism for achieving female-biased sex ratios. Here, we tested this mechanistic hypothesis by varying the risk of male–male competition that male house mice perceived during development, and quantifying sperm sex ratios at sexual maturity. Our analyses revealed that males exposed to a competitive ‘risk’ produced lower proportions of Y-CBS compared to males that matured under ‘no risk’ of competition. We also explored whether testosterone production was linked to sperm sex ratio variation, but found no evidence to support this. We discuss our findings in relation to the adaptive value of sperm sex ratio adjustments and the role of steroid hormones in socially induced sex allocation.

4. Discussion

Recent research has indicated that the sperm sex ratio is a plastic trait that responds to prevailing social conditions [9], which highlights the potential that these adjustments function as a mechanism of male-driven sex allocation [31–34]. In a previous experiment on house mice, we found that exposure to high-male density conditions during sexual development (3–12 weeks of age) resulted in the production of higher proportions of Y-CBS and larger testes [9], which taken together support the male fertility hypothesis [31]. Despite there being strong evidence that low testosterone levels lead to the production of female offspring [45], the precise mechanism by which testosterone influences sperm sex ratios is currently unknown. In the current investigation, we tested whether sperm sex ratio adjustments are linked to variation in testosterone production. Contrary to our expectation, we found that males reared under a risk of competition produced lower sperm sex ratios (i.e. more X-CBS biased) compared with males that matured in the absence of rivals. It is interesting that males exposed to the competitive environment in the current experiment (risk) produced more X-CBS biased sperm ratios than males exposed to the non-competitive environment (no risk), while the opposite result was observed in our previous study (competitive environment = ‘high-male density’; non-competitive = ‘high-female density’) [9]. While these results are seemingly contradictory, differences in experimental design are likely to account for the different responses. The degree of perceived male–male competition was comparatively less intense in our previous experiment (i.e. males maturing within the same room as other males; [9]) than what was applied in the current experiment (i.e. rival males maturing within close proximity to one another within the same experimental tub), which highlights the intriguing possibility that variation in the intensity of competition (and not just presence/absence) leads to different sperm sex ratio responses.

Theory predicts that it would be maladaptive for parents to produce male offspring in a mate competitive environment because they would be forced to compete for access to females and/or be subjected to sperm competition [20]. Conversely, with guaranteed mate availability, high-male density conditions will be evolutionarily favourable for females. Thus, the production of daughters under these conditions is expected to be advantageous to both mothers and fathers [20]. Adaptive maternal sex allocation in relation to male density within the local neighbourhood has been demonstrated in diverse species, including spider mites [21] and house mice [29]. Here, we used house mice sourced from an island population where dispersal capacity is severely restricted and consequently parents and offspring often experience the same local social conditions (see the electronic supplementary material for more information). As a consequence, it is likely that males are forced to compete with both related (sensu local mate competition; [20]) and unrelated males for access to females. We demonstrated that male house mice reared under conditions of intense male–male competition produced higher proportions of X-CBS relative to males not subjected to competition—an outcome that has the potential to have adaptive paternal consequences. Certainly, if increased numbers of female-producing sperm translate to more female offspring, sperm sex ratio adjustments could potentially be an effective strategy for males to enhance their grand-parentage under competitive conditions. We plan to explore this currently untested hypothesis in our future research.

The precise mechanism(s) controlling sex allocation in mammals is currently not well understood. In terms of paternally driven proximate mechanisms, recent research has linked variation in sperm sex ratios [34] and differential X- and Y-CBS motility to offspring sex ratios [46,47]. Further to this, there is evidence to suggest that the ultimate cause of socially induced sex ratio biases involves physiological responses via endocrine signalling [30,48]. Here, we found that the social environment influenced testosterone concentration, but only as a consequence of elevated levels in a subset of ‘risk’ males. Although these individuals produced proportions of Y-CBS at the lower end of the scale, our statistical analyses provided no evidence that sperm sex ratio plasticity is driven by variation in testosterone production. The division in testosterone levels in the ‘risk’ treatment (i.e. less than 20 ng ml⁻¹ and greater than 30 ng ml⁻¹) may be indicative of hormone profiles linked to social status. The default assumption is that social hierarchies are associated with differential testosterone levels, but, in fact, more often than not there is no predictive pattern (e.g. see [49] and references therein). For example, it is only the most aggressive dominant male mice that display elevated testosterone levels (relative to less aggressive dominant males and subordinate males) [49], which likely explains the pattern we have observed in our ‘risk’ treatment. Stress hormones, such as corticosterone, are more commonly associated with social status in male mice, although the direction of the effect has been inconsistent [49]. Offspring sex ratio biases have been linked to maternal stress in a number of mammals [29,30], yet the role that paternal stress plays in sex allocation remains an open question. To address this gap in knowledge, our future research will focus on the relationship between socially induced paternal stress and variation in the sperm sex ratio.