Female snow monkeys like to have sex with other females

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There are numerous accounts of sexual behaviors between females of a primate species called Macaca fuscata, Japanese macaque, or snow monkey (for a review see Vasey, 2002a). There is nothing peculiar with this. Sexual activities between individuals of the same sex are very common among mammals, as mentioned so many times that I start to feel ashamed of repeating it once more. However, one peculiarity with female snow monkeys is that they form temporary female-female associations lasting from less than one hour up to over a week. These associations have been termed 'consortships' (Wolfe, 1983). Typical of these consortships is a rather intense sexual activity where the females mount each other. One study reports a mean of 31 mounts per hour of observation (Vasey, 2002b). Furthermore, while 55% of the females formed this kind of sexual association with other females, only 45% formed sexual associations with males. These data demonstrate that there is a substantial extent of sexual activities between female snow monkeys. Without having quantitative data from other species, I nevertheless assume that such intense same-sex activities are fairly unusual. What is still more peculiar with these monkeys, though, is that there is evidence showing that the females prefer to have sex with each other when an attractive male is also available and even insisting on sex.

The experimental procedures for determining sexual preferences have been varied, but one of the more direct approaches consisted of observing responses to invitations from a male in pairs of females engaged in homosexual activity. These invitations were directed towards one female in the pair, and she had, then, the opportunity to choose between accepting the invitations from the male or continue mounting the other female. In 92.5% of the situations of this kind, the female chose to continue mounting the other female. The male was chosen in only 2.5% of the situations (Vasey, 1998). These data quite convincingly show that female snow monkeys, at least in the population studied, prefer sexual interactions with other females when given a choice. However, this does not mean that females preferring to mount other females will never accept copulating with males. In fact, all females will have one or more sexual interaction with males during the breeding season (Vasey, 2002a). Exactly as was the case with the male-mounting rams, a clear preference for the own sex is evident in certain situations, but that preference does not impede sexual relations with members of the opposite sex in other situations.

It is not at all surprising that the intense same-sex activity described in some populations of female snow monkeys has prompted speculations as to the cause. The most obvious according to popular prejudice, some unusual production of gonadal hormones during early and/or adult life, has not attracted any attention, at least not to my knowledge. On the contrary, cell numbers have been counted in a small region in the vicinity of the preoptic area, the dorsocentral portion of the anterior hypothalamic nucleus. This region, of unknown function, was selected because it is sexually dimorphic in the rhesus macaque (Byne, 1998). With dimorphic is here understood that it is larger in males than in females, not that it is exclusive to one sex or the other. It is a good example of a statistical dimorphism. The reasoning was that the difference between males and females might be smaller in the snow monkey population where females show high levels of same-sex behavior than in the rhesus monkey, a species where female same-sex activity is low or entirely absent. Results showed that the size as well as the neuron counts differed as much between males and females in the snow monkey as it does in the rhesus (Vasey and Pfaus, 2005). It appears, then, that there is no structural peculiarity in a region known for its importance in male sexual behaviors and perhaps also for proceptive behaviors in the female (see Chapter 6).

Rather than attributing the female snow monkeys' habit of same-sex mounting to endocrine alterations or structural quirkiness in some region of the central nervous system, an explanation in terms of learning has been proposed. It is based on a careful analysis of the females' behavior while mounting other females. During mounting, prolonged clitoral contact with some part of the mountee's body is common. This occurs, for example, when performing a sitting mount. This is a mount where the mounter sits on the mountee's back in a jockey-like position, while grasping the mountee's upper back with her hands and the mountee's lower back with her feet. The mounter repeatedly and vigorously rubs her clitoris against the back of the mountee. At another kind of mount, the double-foot clasp, the mounter grasps with her feet between the mountee's ankles and hips, and with her hands on the mountee's back. In that way, the mounter's groin is in contact with the mountee's perineum, thereby stimulating the clitoris of the latter. In addition to procuring these kinds of clitoral stimulation to mounter and mountee, respectively, both females frequently masturbate by rubbing their clitorises with their tails. This short description of same-sex mounts in female snow monkeys is based on accounts by Vasey (1998, 2002) and Wolfe (1983). The important point here is that female-female mounting and associated masturbation provide efficient clitoral stimulation. We may assume that this stimulation produces a state of positive affect and that it can reinforce learning. There are no experimental data showing this to be true, but I would suggest that most women would accept that clitoral stimulation indeed is pleasurable. The fact that the female snow monkey engages in clitoral stimulation should by itself suggest that the effect in macaques is similar to that in women. Otherwise it would be difficult to explain why the females display such an intense mounting activity.

Provided that the clitoral stimulation obtained while mounting other females and while being mounted by another female is rewarding and reinforcing, motor patterns leading to this stimulation should acquire enhanced probability of repetition through operant learning. Likewise, stimuli present during the pleasurable experience should acquire sexual incentive properties through classical conditioning. It is not impossible that stimuli emitted by the female partner are salient in the situation. Thereby they are most likely to get sexual incentive properties. If monkeys emit stimuli such that an individual can be distinguished from other individuals, then a particular female would become the sexual incentive. This is exactly what seems to occur in the consortships mentioned earlier. With the passage of time and the execution of a considerable amount of sexual responses, the incentive properties of this particular female may get reduced because of negative alliesthe-sia or some other behavioral process. The consortship would then end.

The reasoning presented in the preceding paragraphs is not much different from what Vasey (2002a) proposes. 'Once females evolved the capacity to mount, and the capacity to derive sexual gratification during mounts through clitoral stimulation, they could do so just as easily by mounting females, as males' (Vasey, 2002a, p. 173).

In this context, it may be useful to draw attention to the most interesting results of a comparison of the motor patterns employed by female snow monkeys when mounting other females with those employed by males when mounting females. It was found that the males' motor pattern was much more stereotyped than the females' pattern. This was explained by suggesting that the males' mounts were constrained by the requirements imposed by penile-vaginal penetration. There are not so many mounting positions and movements available that assure successful intromission. All motor patterns not leading to intromission can be expected to become extinguished because of lack of reward and reinforcement, leaving only those most likely to produce the rewarding and reinforcing event of intromission. The females, at difference, can attain clitoral stimulation in a variety of ways. Their copulatory motor patterns were frequently far more complex than the males', employing combinations of forward, sideward and upward movements. Presumably, these motor patterns assure abundant clitoral stimulation. They were never observed in males (Vasey et al., 2006).

One conclusion that immediately can be drawn from the exciting study of cop-ulatory motor patterns in the snow monkey just described is that primates have a potentiality for modifying these motor patterns to an extent not seen in other mammals. We can also note that learning may shape these motor patterns in a very important way. It is evident that learning would not be able to have this effect in the absence of some degree of motor flexibility, so the latter rather than disparities in learning ability is probably the cause of this basic difference between primates and other mammals. Furthermore, the snow monkey is the only non-human species where all evidence points to an explanation of same-sex preferences in terms of learning. I suggested that the ram-mounting rams also have acquired their preference through learning, but admittedly there is no experimental evidence supporting that proposal.

The snow monkey is the last example of same sex preferences in unmanipulated animals I will mention. It is so because I know of no other mammalian species where this kind of preferences has been described in a scientifically acceptable way. We might find it amusing to consider the fact that in the two species where we have solid data showing that a significant proportion of a population shows a sexual preference for the same sex, the execution of copulatory acts (mounting) with individuals of the same sex leads to a sexually rewarding and reinforcing event (intromission/ejaculation in the ram, clitoral stimulation in the snow monkey).

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