Male Prudence and Sperm Limits
KeywordsSperm Competition Sperm Number Subordinate Male Cryptic Female Choice Porn Consumption
Males do not maximally inseminate females each mating, but rather strategically inseminate sperm according to intrinsic factors such a body condition and extrinsic factors such as sperm competition risk and female quality.
The root of the evolutionary differences between the sexes is gametic anisogamy, whereby males produce lots of tiny and relatively cheap gametes, while females produce fewer immotile and relatively more expensive gametes. Despite the relative difference in gametic investment between the sexes, males are clearly not always eager to mate, just as females are not always reluctant to mate to protect their high investment. And even when males do mate, they do not always inseminate females with the largest possible ejaculate or best quality sperm that they can make. Instead, ejaculates are often modified according to intrinsic and extrinsic factors (Wedell et al. 2002).
Ejaculatory and Copulatory Adjustment
Adjustment of copulatory investment in males has been known for decades. The Coolidge effect refers to the observation that a male placed in an arena with multiple females will mate repeatedly with all the females up to the point of apparent sexual exhaustion. However, when a new female is introduced to the group, the male will quickly recover and mate with renewed vigor with the new female (Rattus rattus). Males will also adjust their ejaculate investment and inseminate the new female with greater amounts of sperm (Gallus gallus). Such strategic investment makes evolutionary sense. Continuing to mate with the same female would likely be wasteful beyond the point at which the female has either acquired enough sperm to fertilize all of her eggs or has been sufficiently stimulated by the male to use his sperm.
Ejaculate Production Is Costly
The physiological cost of ejaculate production, including sperm and seminal fluid production, can be significant. Therefore, sperm prudence is necessary, as males can be limited in the amount and quality of sperm, as well as the amount and quality of seminal fluid they can produce during a reproductive season (Wedell et al. 2002), and males can lose fitness after repeated ejaculation due to sperm depletion. Ejaculatory investment often varies according to the male’s body condition. When males are in better condition, they can have larger testes and produce higher-quality sperm than when they are in poor condition.
Extrinsic Factors Affect Ejaculate Investment Across Taxa
Ejaculate investment can be influenced by extrinsic factors affecting male mate choice and sperm competition (Kelly and Jennions 2011). Males will inseminate more sperm when they perceive sperm competition to be high (in the presence of a male that can witness copulations by a pair) than when no other rivals are present.
Males also allocate more or better quality sperm to females that will produce a higher fitness payoff to the male investment (Kelly and Jennions 2011). Higher-quality females can include those deemed to be more fecund, unmated, more genetically compatible, and more distantly related (Kelly and Jennions 2011).
The combination of the male’s own quality and the quality of the females available for mating can also mediate ejaculatory investment: Dominant cocks (Gallus gallus) are more prudent in their ejaculatory investment than subordinate males. Dominant males mate more often, and they allocate more sperm to high-quality females, whereas subordinate males have similar ejaculatory investments in the few matings they can achieve.
Ejaculatory Capacity in Humans
Depletion of the extragonadal reserve of sperm in men is rapid, occurring on the second day after an average of 2.4 ejaculations per day, with significant declines in ejaculate volume (47%), sperm concentration (67%), and total sperm (84%) during this period (Freund 1963). During the follow-up period, the numbers of sperm remained well below the original counts before the beginning of the experiment (Freund 1963), suggesting that sperm depletion is a real risk for men after repeated ejaculation and, therefore, that strategic sperm allocation may be evolutionarily favored. Other studies have supported the generality of these findings (reviewed in Shackelford et al. 2005).
Evidence of Ejaculate Adjustment in Humans
In humans, ejaculate adjustment was reported in a study where the authors tested the hypothesis that men may inseminate more sperm to their partners after they had spent time apart, presumably because they could not have mate guarded (Baker and Bellis 1989). Ten couples used a condom to collect ejaculates resulting from intercourse, and their sperm counts were compared to those of ejaculates collected through masturbation. Data from how much time they had spent apart prior to the copulation were collected, and the authors reported that sperm numbers were significantly correlated with the percent time the couples had spent apart prior to copulation, while no such correlation was found for the masturbation samples (Baker and Bellis 1989). In a follow-up study that added a large survey to investigations of ejaculate number, Baker and Bellis again reported a correlation between sperm numbers and time apart prior to copulation, but their sample sizes continued to be very small (out of 33 recruited pairs, only 15 males produced repeated intra-pair copulation samples, and most did not produce masturbation samples) (Baker and Bellis 1993). They also concluded that men inseminate larger numbers of sperm to larger females (heavier and taller), consistent with the idea that males should adjust their ejaculate when mating with higher-quality females. From the survey data on 3,679 women, they concluded that time apart did in fact reflect the risk of sperm competition, as women who reported having extra-pair sex were more likely to do so when they were apart from their partner.
Although their results are intriguing, Baker and Bellis’ studies are correlational in nature, suffer from lack of controls, and small sample sizes (Shackelford et al. 2005; Leivers et al. 2014). Unfortunately, no recent experimental studies with large sample sizes have followed up Baker and Bellis’s studies.
The quality and quantity of ejaculates collected from copulatory activities compared to ejaculates collected from masturbation are known to be different (Shackelford et al. 2005). Although this hints at the potential for strategic sperm allocation to take place to avoid wasting too much sperm during masturbation (Shackelford et al. 2005), better/larger ejaculates may be a nonadaptive consequence of higher levels of arousal during copulation when compared to masturbation. Men produce better ejaculate samples through masturbation when allowed to view erotic materials, again perhaps because such materials produce higher arousal levels.
Perceived sperm competition while viewing erotic materials seems to result in ejaculatory adjustment. Men express a preference for erotic materials that depict multiple males engaged in sex with one female than a single male having sex with multiple females as evidenced by sales of erotic DVDs (McKibbin et al. 2013). This preference seems to be translated into ejaculate quality. When viewing erotic materials, males produced a higher-quality ejaculate when the material included two men and one woman than when it only included three women, presumably because men were viewed as potential competitors (Kilgallon and Simmons 2005). And just as is the case in cocks, ejaculate investment in men can be context dependent, according to the male’s own mate value. Men that were rated as having higher mate value invested more in ejaculates only when viewing erotic images of women deemed to be of higher quality (Leivers et al. 2014).
Men have also been found to produce better ejaculates when exposed to novel females during a porn viewing experience (Joseph et al. 2015), just as predicted by the Coolidge effect. Males were exposed to erotic images of the same woman six times, before being exposed to a novel woman. Contrary to expectations, this study failed to find a decrease in the measured ejaculatory parameters between times 1–6 of exposure, perhaps because the men in the study had ample time to recover between exposures (48–72 h), but the introduction of novelty resulted in a significant increase in sperm motility, and ejaculate volume, and a decrease in ejaculation time (Joseph et al. 2015). The extraordinary success and addictive power of easily available porn in the Internet seem to take advantage of men’s increased sexual interest in young, diverse, and fertile females. More studies are beginning to delve into the patterns of porn consumption in men and whether these can at least partly be explained by our evolutionary history.
it is evident that without repeated specimens under controlled conditions, no estimate of the variation among specimens within donors can be made. Without such an estimate of within donor variation, no conclusive test of the significance of the differences among donors, among fertile and unfertile groups, or among or among treated and control groups, can be made.
Therefore, experiments with larger sample sizes that control for known factors that cause intrinsic variation of ejaculate quality are badly needed to determine the relative importance of strategic sperm allocation and sperm prudence in men.