Another confusing concept sexually dimorphic behaviors

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A point that must be taken into consideration, even if the only purpose is to reject it, is the fact that popular, and frequently not so popular, beliefs maintain that some sexual behaviors are sexually dimorphic in both the human and other animals. There is, indeed, one sexual behavior that we must accept not only as typical of one sex but also as possible only for one sex. I am referring to a class of behaviors usually called penetrative sex and within that class to the acts of the penetrator. The act of sexual penetration requires an erect penis on the part of the penetrator and only men and other males are properly equipped for displaying that kind of behavior pattern. If we exclude women employing plastic surrogates for penetrating other women or men, we need to conclude that the penetrator, or inserter as some like it, is always a male. However, the human male can easily penetrate other males, so being the penetrated, or the insertee as some like it, is not a privilege of women. While inserter behavior is sexually dimorphic, behaviors displayed by the insertee are not necessarily so. Again, just as was the case with oral sex, where it had no importance whether it was directed toward male or female genitalia, penetrating one opening is, in principle, no different from penetrating another, at least not as far as the penetrator (inserter) is concerned. It appears, then, that the only dimorphic sexual behavior is penile penetration. All other sexual behaviors may be displayed by both men and women. It is very tempting to speculate that it is exactly this sexual dimorphism that has made penetrative sex the only legitimate for millennia. Historians may have thought of that possibility.

In non-human animals we have, not surprisingly, another sexual behavior category that might be sexually dimorphic, that of accepting penetration or being the insertee, if we should happen to prefer that expression. There are few reports of male non-human mammals penetrating other males, but it may occur in rams as we will see in a few pages. Nevertheless, it is very unusual. As I pointed out long ago, this is most likely a consequence of the stereotyped nature of copulatory behavior in non-human mammals. While the human male can make use of basic anatomical knowledge to localize usable body openings in other men or in women, nonhuman males seem to have a weaker knowledge of anatomy. Furthermore, it is not sufficient to localize the opening. The penetrating organ needs to be put in contact with it, and entry must frequently be ascertained with the help of hands and sometimes also of artificial lubrication. All these activities are possible for the human male because of his extremely flexible copulatory behavior, combined with his motor abilities and intellectual creativity. On the contrary, none of the necessary supplementary behaviors are easily available to rats, and not even to monkeys and apes, because of a far more stereotyped copulatory behavior and less creativity.

In addition to penetrative sex, some other sex-related behaviors may be sexually dimorphic in several species. For example, hop-darting and ear wiggling are not common in male rats. There are no data as to their frequency in males, but I have to admit that it is rather unusual if not outright exceptional to see a male performing hop-darting or ear wiggling. It is possible that these behaviors should also be considered sexually dimorphic. Independently of this, it is most likely that there are more behavioral sexual dimorphisms in non-human animals than in the human. This can probably be attributed to the stereotyped, not to say reflexive, nature of copulatory behavior in the former.

Although only a few sexual behaviors are dimorphic in the sense that they are displayed by one sex but not by the other, we must admit that some behavior patterns are far more frequent in one sex than in the other. This could be considered as a statistical dimorphism. For example, the likelihood that a sexually receptive female rat will display lordosis when mounted is far above the likelihood that a male rat will display lordosis when mounted (Figure 8.1). Similarly, the likelihood of displaying a mount when exposed to a receptive female is higher in a male than in a female exposed to another female. It is certainly this difference in probability of occurrence that makes some scientists consider mounts as male-typical behaviors and lordoses as typical of females. For convenience I will frequently do the same.

FIGURE 8.1 Left: A male rat mounting a sexually receptive female. Note the female's lordosis posture. Right: The male rat seen in the left panel is now mounted by another male. Please note the male mountee's lordosis posture. Both pictures are still images from a video, making the quality suboptimal.

FIGURE 8.1 Left: A male rat mounting a sexually receptive female. Note the female's lordosis posture. Right: The male rat seen in the left panel is now mounted by another male. Please note the male mountee's lordosis posture. Both pictures are still images from a video, making the quality suboptimal.

The probability of performing a response is not only determined by the sex of the individual, but also by the environmental stimuli present at any moment. No sexual behavior is displayed in the absence of a sexual incentive. It is probable that the sex of the incentive is important for the likelihood of performing a male-typical or a female-typical response. The frequency of mounting is probably lower in male rats exposed to other males than in males exposed to receptive females. The display of lordosis in females is probably less likely when mounted by a female than when mounted by a male. Likewise, female proceptive behaviors are probably more likely when exposed to males than when exposed to other females. Experimental data unequivocally supporting these suppositions are not available, but this is perhaps not crucial for the moment. The important point here is that the sex of the incentive, in addition to the sex of the individual reacting to the stimuli emitted by the incentive, may determine the likelihood of occurrence of a particular behavior.

The rather complicated interaction between incentive and the behavior displayed as well as a classification of these behaviors was the subject of a brilliant chapter by Frank Beach (Beach, 1979). He suggested that the behavior displayed by a male mounting a female should be called normal, regardless of whether the female was receptive or not. On the contrary, the behavior displayed by a male mounting another male should be called homosexual. The mounted male's behavior was called normal if he resisted or remained passive and homosexual if he responded with lordosis. A female mounting another female shows homosexual behavior independently of whether the mounted female responds with lordosis or not. Finally, the behavior shown by a female mounting a male is given no name at all by Beach. This is also the case for behaviors shown by a male in response to a female's mount even if he should happen to respond with lordosis. Beach goes on suggesting that the label 'homosexual' is not very illuminating. I do agree. Instead, the 'sex' of the motor pattern should be considered. With that is understood that a mount is a male motor pattern while lordosis is a female motor pattern. I do not agree. It is probably true that mounts are more frequent in males than in females, and it is certainly true that lordoses are more frequent in females, something I

already insisted upon. Despite the differences in frequency of appearance, I find it more convincing to call a mount a mount regardless of the sex displaying it. It is particularly so since a mount performed by a male and a female are identical motor patterns, as was made evident in the section describing sexual behaviors in Chapter 2. This same argument applies to lordosis. The behavior pattern should be called lordosis independently of the sex of the individual performing it. There is no reason to believe that a lordosis performed by a female is any different from that performed by a male. I admit that Beach's (1979) proposal to move away from the term homosexual was a good one. However, the replacement terms he suggested, 'homotypical' or 'heterotypical', do not contain any useful information, so far as I can judge. The time has arrived to move away from these expressions and stick to terms describing the behaviors themselves without adding any value-laden labels.

We may intuitively have noted that the assumption on which terms like 'homosexual behavior' or 'homotypical behavior' rest is that sexual behaviors indeed are sexually dimorphic. We have noted that, in the human, this is correct only for the behavior displayed by the inserter while inserting. In other mammals, that behavior plus the one displayed by the insertee while being inserted are the only indisputable cases of sexually dimorphic behaviors in the strict sense of dimorphism. We forget about proceptive behaviors for the moment. If we accept the notion of a statistical dimorphism, we may indeed accept that the main elements of nonhuman, particularly rodent, copulatory behaviors, mount and lordosis, are dimorphic. At the time of Frank Beach's (1979) analysis, it was entirely respectable to regard mount and lordosis as dimorphic behaviors because of sex differences in the frequency of occurrence. However, since then we have learned much more regarding lordosis in male rats and mounting in female rats. Freud's visionary notion of a fundamental, universal bisexuality has received so much empirical support in empirical studies of non-human animals that the concept of dimorphisms in sexual behaviors is, as I have argued for a couple of paragraphs by now, not really meaningful anymore. With the demise of that concept, terms like homo-typical and heterotypical must also disappear. We will soon turn to one example of the kind of experimental observations that has contributed to this. Actually we will do that now.

Most valuable data concerning the issue of classification of sexual behaviors in old fashioned categories like homosexual and heterosexual or homotypical and heterotypical come from a series of exciting studies by Jim Pfaus and colleagues at Concordia University in Montréal. They decided to analyze female mounting behavior in more detail than has ever been done before. The requisite for being able to do so was, obviously, the use of a situation where female mounting is readily shown. Not all experimental situations permit the female to express mounting behavior. For example, during sexual interactions with an active male, the female is normally kept busy displaying proceptive behaviors and lordosis in response to the male's approaches and mounts. Moreover, sexually active males do not easily accept being mounted. This means that there is little opportunity for the female to present mounting behaviors. An alternative would be to evaluate female mounting behavior in same sex pairs. This has been done in many studies and, although female mounting is not unusual in this situation, its frequency is rather low. In contrast, females show high levels of mounting when exposed to non-copulating males. Such males are easily obtained by castrating a group of animals and then selecting those that do not show any copulatory behavior at all after a few weeks. When ovariectomized females are paired with non-copulating males, almost no female mounting is observed. However, after treatment with estradiol with or without progesterone, the number of mounts increased substantially. Progesterone without estradiol was ineffective. These results show that mounting is dependent on estrogens. The role of progesterone is uncertain, but an estrogen + progesterone synergy cannot be excluded until low doses of estradiol have been tested. Data from a group of cycling females confirmed the importance of ovarian hormones. There was a sharp increase in the number of mounts at proestrus. What is particularly important in the present context is the conclusion, which I will cite literally: 'Thus, mounting behavior may not be sexually dimorphic but rather guided by certain external and internal stimuli that both sexes are sensitive to' (Afonso and Pfaus, 2006, pp. 36-37). In subsequent papers, it was shown that the external stimuli determining the occurrence of female mounting were similar to those controlling mounting in males (Afonso et al., 2006a, 2006b). This series of studies suggests that Beach's (1979) refusal to put a label on the behavior shown by a female mounting a male was unwarranted. There is no reason why it should not be called mounting. The addition of the adjective heterosexual to the noun mounting does not seem to add any further information. Moreover, the results of the studies from the Pfaus group certainly reinforce the notion I have already put forth several times, namely that neither mounting nor lordosis should be considered as sexually dimorphic behaviors.

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