From 2013... Effect of mating activity and dominance rank on male masturbation among free-ranging male rhesus macaques. Constance Dubuc, Sean P. Coyne, and Dario Maestripieri
Ethology. 2013 Nov 1; 119(11): 10.1111/eth.12146.
Abstract: The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non-human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale-multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non-functional by-product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free-ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower-ranking males mated less and tended to masturbate more frequently than higher-ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.
Keywords: Masturbation, auto-erotism, male-male competition, sexually-transmitted disease, sexual arousal, mating success, dominance rank, rhesus macaques
INTRODUCTION
Masturbation, or self-manipulation of the genitalia, is part of the natural behavioral repertoire of many animal species (reviewed in Bagemihl 1999; Thomsen et al. 2003; Dixson 2012), including humans (Laqueur 2003; Dixson 2012), but whether this behavior has an adaptive function is still poorly understood. Although comparative behavioral data on masturbation could help us understand the adaptive function and evolution of this behavior, very few data are available to date.
Different hypotheses have been proposed to explain the function of male masturbation (reviewed by Waterman 2010; see also Dixson 2012). The “sexual-outlet” hypothesis proposes that masturbation is a non-adaptive by-product of sexual arousal and serves as an alternative outlet to copulation (Kinsey et al. 1948; Dixson & Anderson 2004; Dixon 2012). This by-product hypothesis implies that males do not gain any fitness benefits, in terms of their health or survival, or increased mating or reproductive success, from masturbation. Second, the “ejaculate-quality-improvement” hypothesis posits that masturbation is an adaptive behavior that serves to eliminate degraded gametes or avoid polyzoospermy in order to increase the overall ejaculate quality, thus increasing the probability of impregnation when males copulate with a fertile female (Zimmerman et al. 1965; Baker & Bellis 1993, 1995; Thomsen et al. 2003; Thomsen & Soltis 2004). While suggesting very different functions of masturbation, these two hypotheses both predict that masturbation should be more frequent among males that have little or no opportunity to mate, and/or occur in periods of infrequent mating (Thomsen et al. 2003; Thomsen & Soltis 2004; Dixson & Anderson 2004; Waterman 2010; Dixon 2012). In addition, the ejaculate-quality-improvement hypothesis predicts that males who have infrequent access to females but masturbate frequently should have higher sperm quality and higher probability of impregnation when compared to males who masturbate less frequently, other things being equal. Finally, according to the “STI-reduction” hypothesis, masturbation serves to cleanse the male reproductive tract to decrease the risk of contracting sexually transmitted infections (STIs) (Waterman 2010). This hypothesis has been developed more recently to explain the behavioral pattern observed in the highly promiscuous Cape ground squirrels (Xerus inauris; Waterman 2010). Contrary to the two other hypotheses, the STI-reduction hypothesis predicts that male masturbation should be more prevalent in periods of high sexual activity, performed by males who mate successfully, and occur shortly after copulation (Waterman 2010). Moreover, it predicts that males who masturbate frequently in these circumstances should be less likely to contract sexually transmitted diseases than males who do not masturbate or do so less frequently, and should thus be in overall better health. It should be noted that all three hypotheses are based on the assumption that male masturbation typically leads to ejaculation.
Among nonhuman primates, the occurrence of male masturbation has been documented at the qualitative level for 30 species of Old World monkeys and apes, whereas it is rare or even absent in New World monkeys and prosimians (reviewed in Thomsen et al. 2003; Dixson 2012). Male masturbation is most frequent in anthropoid primates that live in multimale-multifemale groups (Thomsen et al. 2003) and have large testis volume relative to their body size (Dixson & Anderson 2004). While this observation has been interpreted as being suggestive that male masturbation is functionally linked to sperm competition (ejaculate-quality-improvement hypothesis; Thomsen et al. 2003), this observation is also consistent with the sexual-outlet hypothesis because in sexually promiscuous species “males possess neuroendocrine specializations for greater sexual arousal and performance” (Dixson & Anderson 2004, p. 366; see also Dixon 2012, p. 192). Such pattern could also be explained by the STI-hypothesis because sexually transmitted infections are more likely to spread in species with promiscuous mating system (Waterman 2010).
While no primate studies to date have directly investigated the potential fitness benefits of male masturbation, a handful of studies have investigated the functional hypotheses indirectly, by testing their predictions concerning the frequency of masturbation and its potential association with rank and mating activity within species. In free-ranging red colobus monkeys (Procolobus badius), masturbation was performed very rarely (5 instances in 8,950h of observation collected over 5 years) mainly by alpha males and specifically during intergroup encounters (i.e. when rivals are present) taking place when some females were sexually active, with no copulations reported for either resident or extra-group males (Starin 2004). Male masturbation was much more frequent in two macaques species, in which hundreds of instances were observed over less than 1000 hours of observation collected over 1–2 years (Nieuwenhuijsen et al. 1987; Thomsen & Soltis 2004). In free-ranging Japanese macaques (Macaca fuscata), masturbation is more frequent in males of lower mating success and those of lower dominance rank (Thomsen & Soltis 2004; see also Inoue, 2012). No such relation between dominance rank and masturbation frequency was revealed in captive group-living stump-tail macaques (M. arctoides; Nieuwenhuijsen et al. 1987). A closer investigation of the latter study’s data, however, revealed an opposite pattern of distribution of mating and masturbation rate between the alpha male (409 copulations vs. 30 masturbation bouts) and the beta male (30 copulations vs. 543 masturbation bouts), which suggests a relation between rank, mating, and masturbation similar to that reported in Japanese macaques (cf. Table 3 in Nieuwenhuijsen et al. 1987). Overall, the results obtained for macaques seem more consistent with the ejaculate-quality-improvement and sexual-outlet hypotheses than with the STI-reduction one.
In the present study, we examined whether and how access to fertile females influences masturbation rate in free-ranging male rhesus macaques on Cayo Santiago, Puerto Rico. Rhesus macaques are seasonal breeders and on Cayo Santiago that they live in unusually large troops (50–300 individuals). In this rhesus population, male mating and reproductive success are linked to dominance rank, although not strongly (e.g. Berard et al. 1994; Dubuc et al. 2011). High-ranking males form extended consortships with estrous females characterized by frequent copulations and ejaculations, while lower-ranking males mate less frequently and mainly through sneak copulations and short-term associations (e.g. Carpenter 1942; Altmann 1962; Chapais 1983; Berard et al. 1994; Higham et al. 2011). However, middle- and low-ranking males can still enjoy a relatively high reproductive success (e.g. Berard et al. 1994; Dubuc et al. 2011) because high-ranking males are generally unsuccessful at mate-guarding females over the entire course of their fertile phase (Dubuc et al. 2012), thus making it possible for other males to fertilize females through sneaky copulations and sperm competition (see also Bercovitch 1992). While male masturbation has long been known for this species (e.g. Carpenter 1942; Phoenix & Jenson 1973), little is known about the relationship between masturbation and mating activity. Work on captive rhesus macaques has shown that male masturbation takes place even without any sensory contact with females (e.g. Phoenix & Jenson 1973), is eliminated by castration (Phoenix & Jenson 1973; Slimp et al. 1978; Loy et al., 1984), but not by brain lesions that eliminate sexual interactions with females (Slimp et al. 1978).
Here, we explored the possible functional significance of male masturbation by investigating the correlation between masturbation frequency and male dominance rank, and investigating how mating activity influences masturbation behavior in two different ways, by testing (i) whether there is a correlation between masturbation rate and overall mating frequency, and (ii) whether or not males were more likely to masturbate on days in which they were seen mating. Based on previous findings obtained in macaques, we predicted that the pattern of male masturbations will be more consistent with the sexual-outlet and ejaculate-quality-improvement hypotheses than with the STI hypothesis. Specifically, we predicted that (1) low-ranking males and/or least successful males of a social group should be more likely to be observed masturbating, and (2) males should be more likely to masturbate on days in which they do not mate. In addition, we expected (3) masturbation to lead to ejaculation.
DISCUSSION
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In our study, masturbation that did not lead to ejaculation took place in two main contexts (25% of all masturbation bouts each): (1) males manipulated their in penis only once in a period of time in which they emitted a large amount of self-directed behaviors; and (2) males stopped masturbating and started interacting with females in a sexual context, a third of which led to mating (Fig. 3). In the remaining cases, the male changed activity or simply stopped with no obvious change of activity. Based on these observations, we propose two hypotheses to explain male masturbation in rhesus macaques. Firstly, we propose that it may be a form of self-directed behavior emitted in context of intense anxiety (Maestripieri et al. 1992), which could or could not be created by a sexual context itself (‘masturbation-as-SDB’ hypothesis). Masturbation could be more frequent among low-ranked males if their position creates more emotional stress. Alternatively, male masturbation could be aimed at maintaining high level of sexual arousal for males in order to decrease the length of the next mount series and increase the probability of ejaculating through mating (‘sexual-arousal’ hypothesis). In rhesus macaques, mount series can last from 1 to 56 minutes, and long series are more likely to be interrupted by higher-ranking males (Manson 1996). This would be more frequent among non-dominant males that have a low access to females and mate mainly during short-term associations and sneak copulations.
An unequivocal rejection of the null hypothesis that male masturbation is a non-functional by-product of frustrated sexual arousal would require evidence that inter-individual variation in masturbation behavior is associated with variation in male health, emotional stress, ejaculate quality, and/or in fertilization success. While Inoue (2012) showed no correlation between masturbation rate and reproductive success, the fact that mating rate or dominance rank was not taken into account provides little insights about whether males masturbating produced more offspring than predicted based on their mating rate. Some insights into the function of masturbation could also be provided by comparing closely-related primate species that live in multi-male multi-female groups that differ in the extent to which the alpha male effectively monopolizes access to fertile females (and in turn, the intensity of sperm competition) or in their mating pattern (i.e. multiple-mounters vs. single-mounters). Comparing prevalence of male masturbation, the frequency at which it leads to ejaculation, and context in which it takes place within these species could shed some light on whether maintaining a steady supply of high-quality sperm through frequent masturbation is needed to take full advantage of rare opportunities for copulation that become available to individuals who are otherwise consistently prevented from copulating.
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