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Biological Structures and Male Homosexuality

Many evolutionists (Gould 1977b; Rieppel 1992; Reichholf 1992; Antinucci 1990) have complained about the emphasis placed by sociobiologists on natural selection to the detriment of questions of biological structure. According to these authors, sociobiologists have an overly "atomistic" approach to evolution, acting as if specific biological traits can evolve all by themselves, without regard to structural constraints on design or to the possibility that given structural changes may or may not be possible in phylogenetic history. Tracing structural variations is important because natural selection does not operate like an architect, drawing up a blueprint for a house, and then putting it together from scratch in the most efficient way possible. Rather, natural selection operates more like a "tinkerer" taking advantage of materials already available to produce new forms that "work" at the moment.

The heterozygous theory of homosexuality proposes that genes that affect submissiveness also affect homosexuality. This suggests that the key to understanding homosexuality may lie in the evolution of submissive behavior. We are unlikely to find many clues in the fossil record, but a search for homosexual analogues and homologues in other animals may be informative. Sexual relations between males can be found even in very simple species. In his review of animal homosexuality, Sommer (1990) mentions the case of "homosexual rape" in a parasitic worm (Moniliformis dubius). In this case, the raped male's genital opening is blocked off with a spermless semen plug donated by the rapist. The raped male cannot then fertilize females. A variation on this theme is the homosexual rape of the bedbug Xylocaris maculipennis. In this case, instead of blocking up the rival male's genital opening, the raping male inserts his own sperm into the rival male's semen ducts. This also occurs with fresh water snails of the genus biomphalaria, that are vectors for schistosomiasis (Forsyth 1991). When the raped male copulates with a female, he fertilizes her with his rival's sperm.

Very different is the "homosexual" behavior found in the ten-spined stickleback fish. During spawning activities the male must court a female in order to get her to lay her eggs. Sometimes a second female is invited into the courting arena, and then the male may succeed in fertilizing the eggs of two females. But sometimes the second "female" is really a transvestite subordinate male, who, because of his disguise, succeeds in entering the rival's arena and fertilizing himself the female's eggs, or at least in eating the already fertilized eggs (Sommer 1990). A variation on this theme is found in the bluegill sunfish. In this species there are three different types of males.

First is the larger "parental" male, who defends a nest or courting arena. Second, is the much smaller "sneaker" who sometimes succeeds in darting into a parental's courting arena and fertilizing the female's eggs before the larger male perceives him. Third are the "transvestites" who resemble female bluegill sunfish, and manage to get invited into the arena (Wilson 1994). As they grow, the "sneakers" gradually turn into "transvestites," but the "parental" males are genetically different. That "transvestite" behavior may also be structurally related to homosexual activities is shown in the case of the lizard Anolis garmani. In this animal the main perceived difference between males and females is size. Small males are usually driven out of the territories of larger males, but much smaller males are sometimes confused with females. On entering a more dominant male's territory, these small males behave like females and let themselves serve as sexual partners to the larger males. This trick not only gives the subordinates access to the dominant's territory and to his females, but also succeeds in making the dominant male "waste" his sperm.

A similar ploy is used in forest salamanders subordinates succeed in tricking dominant males into giving up their sperm packets (Sommer 1990), and by male Manitoba garter snakes (Thamnophis sirtalis parietalis) who give off female scents that attract other males into giving up their sperm.

Some of these examples of "homosexuality" in phylogenetically distant animals may be analogous rather than homologous to human homosexuality, but as we move closer to humans the likelihood of homologous behaviors increases. In mammals many different behaviors have been observed that might be associated with male homosexuality. Among primates homosexual behaviors are particularly diverse. These include such practices as the mounting of one male by another (e.g. Langurs, pig-tailed macaques, baboons, orangutans, chimpanzees, bonobos) (Sommer 1990; Oi 1991; Lorenz 1963; Yamagiwa 1992; Hayaki et al. 1989), including mounting with anal penetration (e.g. stumptailed macaques, squirrel monkeys) (Sommer 1990; Maple 1977), and mounting with anal penetration and ejaculation (Japanese macaques, rhesus macaques, gorillas) (Sommer 1990; Gadpaille 1980; Edwards and Todd 1991).

Masturbation of other males has also been reported, including mutual masturbation (e.g. stump-tailed macaques) (Sommer 1990) as well as genital-genital contacts (e.g. bonobos) (Enomoto 1990), at times leading to ejaculation (e.g. gibbons) (Edwards and Todd 1991). Fellatio has also been reported for stumptailed macaques (Sommer 1990). Other perhaps related behaviors include sniffing/inspecting the genitals/anal region of other males (e.g. stumptailed macaques) (Sommer 1990), "displaying" an erect penis to other males (e.g. vervet macaques) (Henzi 1985), and urinating a few drops on the other male during the display (e.g. squirrel monkey) (Castell 1969). In some cases males have shown a preference for their homosexual partners over heterosexual partners (e.g. rhesus macaques) (Sommer 1990).

These behaviors have been reported for a diversity of situations most notably in displays of dominance and submission, in cases of general excitation, and in more playful situations among adolescent males and between adult males who demonstrate special affective relationships with each other.

At first glance the relationships between the different behaviors and the situations in which they occur seem arbitrary. For example, in some cases it is the dominant or older male who mounts the younger or subordinate (e.g. gorilla) (Yamagiwa 1992), in other cases it is the reverse (e.g. pig-tailed macaque) (Oi 1991). Presenting the anal region to another animal may indicate one's dominance (e.g. squirrel monkey) (Ploog et al. 1963), or it may be a submissive gesture (e.g. baboon) (Lorenz 1963). It may be the dominant who sniffs/licks the subordinate adolescent's genitals (e.g. howler monkeys) (Young 1983), or the subordinate who sniffs/licks the dominant (e.g. Hapalidae) (Epple 1967). It may be the dominant who ejaculates (e.g. squirrel monkey) (Ploog et al. 1963) or the subordinate adolescent (e.g. gibbons) (Edwards and Todd 1991). In some cases it is the dominant individual who urinates (e.g. squirrel monkey) (Castell 1969). In some cases the reverse (e.g. a subordinate wolf may urinate on itself) (Lorenz 1963).

The different sexual activities and their social associations seem so diverse that one is tempted to conclude that more complex animals have simply evolved a "flexible" sexuality that allows them arbitrarily to find virtually anything sexy. Indeed, phenomena like the occasional sexual imprinting on different species or even on objects would seem to confirm this view (Maple 1977; Lorenz 1963). Still, I think it possible to find order behind this chaos. We just need to look a little more closely in order to see the structural similarities.

I suggest that male homosexuality may have evolved through various stages. The most primitive stage occurs in animals without multi-male groupings, and where males are generally intolerant of the presence of any other adult male. It would be expected mostly where animals do not recognize each other as individuals, but only as members of categories. Thus there are no "personal" relationships. In this stage, homosexuality is basically a deception tactic to gain access to others' territories (although the animals do not know they are practicing deception or being deceived). This is the stage of the "transvestite" lizards and snakes described above. Possibly such transvestite behavior may be a pre-condition for the use of sexual "mounting" to express dominance in more complex animals. The connection may have something to do with how males succeed in imitating females. Lorenz (1963) gives the example of Cichliden fish. Males recognize females only by the fact that females can mix the emotions of fear and sexual excitement while males cannot. He argues that many vertebrates distinguish between the sexes only by the different ways males and females mix basic emotions. Allowing oneself to be sexually mounted is then associated with submission.

A more complex stage of homosexuality occurs where multi-male groups are adaptive, perhaps in avoiding victimization from predators or for other reasons, but where males do not cooperate with each other on specific tasks. In this situation, more powerful males may have some incentives for expulsing other males, but they also have at least some incentive for allowing them to stay. The "solution" to this dilema is the maintenance of a clear dominance hierarchy. The subordinates can stay in the group, but must periodically "pay homage" to the dominant to clarify their provisional "guest" status. The rituals used to define this dominance may derive from various sources. One source is the behavior used to mark off territories. Many animals have scent glands (often near the genital-anal region) that take advantage of urine or feces secretions to deposit scents on a territory's borders or elsewhere. When subordinate males are allowed to stay near a dominant male, part of the price may be having these territorial markers literally "rubbed in their faces".

For example, Epple (1967) describes the genital displays (perhaps best described as "mooning") among dominant males in different callitrichidae species. In M. a. argentatus the dominant male may, with a threatening face, show its anal-genital region to a subordinate, who crawls with gestures of anguish to the dominant male, and, while emitting submissive sounds, then smells the dominant's genitals. When extremely fearful, submissive males may smell only the dominant's tail. Sometimes the dominant male backs into the submissive and rubs his genitals in the submissive's fur, thus marking the subordinate directly with his own markers. Often the dominant withdraws his testicles, but shows an erection during these displays. The dominant's erection may serve to clarify that he is allowed to have an erection (and sexual relations with females), and the subordinant must get used to seeing this. The subordinant is not permitted this licence.

Squirrel monkeys have similar, but somewhat more complex dominance rituals. The dominant male approaches a subordinate, opens his thighs (sometimes while touching the subordinate with his hands and/or penis) and "displays" his erect penis in the subordinate's face, sometimes emitting a few spurts of urine in the process. The subordinate usually hunches over and may succeed in turning his face away from the display, but if he does not remain sufficiently passive or tries to move away, the dominant may become enraged and aggressive (Castell 1969; Ploog et al. 1963). The relationship between these displays and sexuality involves more than just the fact that erect penises are being displayed. Among mouse lemurs, for example, exposure to the urine of an active dominant male reduces the testosterone level of adult males (Stoddart 1990), which plausibly may reduce their sexual activities. Male prairie voles, exposed to male urine, delay their sexual maturation (Forsyth 1991).

At least for the squirrel monkey, there is clear evidence that the subordinate animals engage in less sexual activity (Ploog et al. 1963). In its genital displays, the squirrel monkey is very similar to the Callitrichidae. But the squirrel monkey has a more complex repertoire. In addition to genital displays, dominants also demonstrate their status by mounting submissives, including anal penetration. Possibly, an ancestral "transvestite deception" system combined with a "scent-marking" system to produce the squirrel monkeys' dominance rituals. Or perhaps the ancestral shows of erect penises simply become more explicit. In any case, the squirrel monkey's dominance system also has other novelties. Dominant males sometimes "ask" other males to stay. They do this by rolling on their backs and exposing their bellies, sometimes showing an erect penis. Animals that would normally run away, stay around if the dominant performs this ritual. This makes for a slightly more cohesive male group than occurs among the callichitridae.

A particularly dramatic variant of the genital display is found in vervets (Henzi 1985). Vervets have bright red penises with powder blue scrota. During submissive gestures, males retract both their penises and their scrota into their bodies, while the dominants leave both extended. In one display, the dominant walks or runs toward the submissive and then turns perpendicular to him so he can observe the dominants' genitals, which the submissive always does. In another, the dominant circles around the submissive showing his anal/genital region, sometimes holding on to the submissive during the display. In addition to these non-solicited displays, the submissives sometimes seek out the dominants in order to "pay homage" to them. They do this by submissively running after them, or creeping up to them, and at times cupping the dominant's testicles in their hands and tugging. Both dominants and submissives have been observed with erections during these latter rituals. Other multi-male species also show "homage-paying" behavior. Lorenz (1963) describes an incident in which a defeated baboon chased after his conqueror "presenting" his behind until the dominant finally mounted him.

I think the different rituals of the Callitrichidae versus the squirrels, and vervets reflect different levels of male/male cooperation. Compared to the callitrichidae, the others seem to have clearer more stable hierarchies. Among the vervets the dominants are confident enough that they can leave their testicles descended during the displays while the callitrichidae bring them out of harm's way. That squirrel monkeys invite fearful subordinates to stay around, and let them show erections also suggests more value given to maintaining the multi-male groups. More stable positions may help explain some of the apparently "contradictory" rituals of different dominance systems. For example, among pig-tailed macaques submissives have been observed mounting the dominants more than the reverse (although it is the dominant who solicits this behavior). Yet immediately after a new monkey rises to the top, it refuses to let others mount it, perhaps because this an especially unstable moment (Oi 1991). This may also help explain why among white-handed gibbons an adolescent was observed soliciting sexual contact with the adult male in his family group. As Edwards and Todd (1991) suggest, the adult may have been "reassuring" the young male that he was still welcome in the family.

In many of these primates immature males seem to "practice" these dominance rituals, displaying or presenting to each other and allowing their partners to mount them (e.g. vervets, rhesus, gorillas, orangutans). This youthful play may be the beginning of what in even more socially complex species becomes an affective type of adult homosexuality, in which neither partner is dominant to the other. "Neoteny" is a common way for "new" traits to appear in a species (Gould 1977a). Adult bonobos, for example, often cement alliances with homosexual activities (Waal 1989).

By way of conclusion, there are a few important points to be made about primate homosexuality. The first is that in all cases, the homosexual behavior has a pacifying effect either averting aggression, reassuring subordinates of their place, or cementing alliances. Also, the different forms of homosexuality seem to "scale", that is, the behaviors and associations found in the simplest species are also found, under certain circumstances, in the more complex animals. But the more complex animals have some additional complications not-present in the others. If this scaling is correct, then this suggests that homosexuality is closely tied to the evolution of more complex social behavior probably via its effect in reducing hostilities between males. What does all of this imply, then, about human homosexuality?

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