The demon within. Part II

Preferential binding by Candida albicans to various types of cells in a macaque brain (Denaro et al., 1995).

In my last post, I examined the relationship between sexual behavior and vulvovaginal candidiasis (VVC), a condition that occurs when certain strains of vaginal yeast (Candida albicans) become highly virulent. Clearly, the relationship is not a simple one of cause and effect. Occurrence of VVC correlates not with vaginal sex but rather with non-vaginal sex, i.e., fellatio, cunnilingus, and masturbation. There is also no significant association between VVC and the presence of C. albicans in the male partner, including his oral cavity.

The evidence suggests that the direction of causality runs in the opposite direction. These strains of C. albicans do not enter a woman’s vagina via fellatio, cunnilingus, or masturbation, at least not primarily. Instead, they may be manipulating the host’s behavior by weakening her sexual inhibitions and inciting her to maximize contact between vaginal fluids and colonizable sites on her partner’s body.

This scenario is all the more likely because vaginal yeast is common and thus provides a large pool of organisms for natural selection to act upon. Vaginal strains of C. albicans also show evidence of adaptation to saliva-based transmission, i.e., they adhere better to saliva-coated surfaces than do other strains (Schmid et al., 1995). In the male partner, they tend to displace non-vaginal strains (Schmid et al., 1993).

So these vaginal strains became better at spreading from a female host to a new male host. But what then?

Did they then evolve the capacity to make the male host more sexually promiscuous? Perhaps. But keep in mind that male-to-female transmission is much less effective than female-to-male transmission. Although VVC can develop on male body sites, the vagina is by far the primary site for C. albicans colonization and infection.

From the standpoint of C. albicans, the optimal scenario would be one where the female host goes on to infect other males. What can her regular male partner do to bring this about?

He could cease all mate-guarding behavior. In plain English, he could stop being jealous. He could even encourage her to have sex with other men.

This kind of parasite manipulation does occur in one organism, the isopod Caecidotea intermedius. A parasite, Acanthocephalus dirus, infects this isopod as an intermediate host in order to enter its final host, one of several freshwater fishes. When the parasite is still soft and immature, it cannot survive a fish eating its isopod host. It thus seeks to reduce this risk by suppressing conspicuous host behaviors, like mate guarding. Later, when the parasite becomes hard and mature, it can survive consumption of its host and, in fact, seeks this outcome. It now stimulates conspicuous behaviors, like mate guarding, and changes its host’s pigmentation to increase visibility (Mormann, 2010).

‘Cuckold envy’

In humans, suppression of mate guarding seems to match a behavior called “cuckold envy”—a sexual fetish where a man is not only indifferent to being cuckolded but actually derives pleasure from cuckoldry. How prevalent is this fetish? A Google search for the term “wife breeding” turned up 793,000 hits, many of which corresponded to videos that have been specially developed for this market.

Cuckold fetishists tend to center their fantasies on black men, perhaps because darker skin and heavier facial features help evoke the image of a rival male. In fact, some of these fetishists have rebranded themselves as members of the “interracial community,” presumably to gain social acceptance and to blend into the broader antiracist movement. Such individuals may be behind the apparent mainstreaming of interracial porn, as seen for example in the antiracist Swedish video Blanda Upp! (2010). One might draw parallels here between lesbian activists and the feminist movement …

This sexual fetish seems to be sufficiently common to foster speculation about a possible Darwinian (or pseudo-Darwinian) cause:

In his book Sperm Wars, biologist Robin Baker speculated that the excitement and stimulation of the cuckolding fetish emerges from the biology of sexuality and the effects of sexual arousal on the brain. According to his theory, when a man believes that his female mate may have been sexual with another man, he is prompted by biological urges to copulate with the female, in an effort to "compete" with the other man's sperm. (Cuckold – Wikipedia)

Baker’s theory fails to explain why most men have precisely the opposite emotional reaction, i.e., feelings of hurt, anger, and rage.

This seems to be true in all human societies. A search for the term ‘cuckold’ in the Human Relations Area Files (HRAF) turned up references to 32 cultures. All of the references indicated intensely negative feelings in the cuckolded men, as seen in the following examples:

Yanomamö (South America)
Discovery of liaisons by the cuckold inevitably leads to club fighting between the factions of the lover and the husband. The woman involved usually suffers more than either of the male principals in the fighting that follows, as women are severely punished by their husbands. The punishment usually consists of a beating with a club, but men frequently shoot their unfaithful wives with barbed arrows in a non-vital area of the body, such as the buttocks or leg. In one instance I witnessed, the enraged husband struck his wife in the face with a burning log, severely burning her mouth. Burning is a common punishment, and many women bear immense scars from wounds inflicted by enraged husbands. (Chagnon, 1967, pp. 91-92)

Tukano (South America)
Adultery or even flirting with a ceremonial friend’s spouse is a principal cause for a break in this otherwise very stable relationship. A ceremonial friend who has been wronged by his partner retaliates by entering the offender’s house to break or carry off everything belonging to him except the hammock. This act of vandalism declares the friendship broken. Eternal animosity succeeds it. (Goldman, 1963, p. 132).

Quechua (South America)
The two strongest insults that Saraguro males can fling at each other (or curse behind their backs) are maricón (homosexual) and cabrón (literally, he-goat, but meaning cuckold). (Belote, 1978, p. 79)

Pashtun (Asia)
[…] for daows (“cuckold” and by extension “dupe”) is the most serious curse and adultery rather than incest the crime of horror. Among the most serious offenses against Pakhtun social order, adultery causes more trouble, mobilizes more sanctions, and ramifies further than any other Pakhtun delict. (Anderson, 1982, p. 401)

Greeks (Europe)
Conversely, the act of disobedience by which she damages her husband most severely is adultery. In adultery she makes her husband a cuckold (κερατ□ς), one who wears a horn. ‘She puts horns on him’ (το□ βάζει κέρατα), it is said. The implication that the cuckold wears a horn may be an ironical allusion to the sexual potency which his wife's action suggests he does not possess (Campbell, 1964, p. 152)

Azande (Africa)
[…] he is certain that she has a lover and he broods in dark anger till he can discover who has made him a cuckold. (Evans-Pritchard, 1937, p. 268)

Men seem to tolerate cuckoldry the most in societies with low paternal investment, i.e., ‘female farming’ societies of sub-Saharan Africa and Papua-New Guinea. But I found no HRAF reference to men actually feeling pleasure at the idea of being cuckolded. The closest match was the custom of ‘wife exchange’ among the Inuit and some Amerindian peoples, like the Comanche:

In many cases, the levirate as practiced by the Comanches approximated polyandry, for brothers lent each other their wives. This “anticipatory levirate” reflected an attitude of camaraderie and denial of sexual jealousy between two brother-warriors.

[…] Women, however, were not free to initiate liaisons. Adulterous men could be sued for damages and customarily made payments in horses or other goods, but the women in question bore the brunt of the shame, and her punishment might include disfigurement (usually slitting of the nose) or death at the hands of her husband. When pressing his case, the cuckold would address his wife's lover as “brother,” an ironic reference to the proper conditions for wife sharing. (Gelo, 1986, pp. 29-30)

When I switched from a cross-cultural search to a cross-historical one, the oldest references to cuckold envy seemed to be in plays from 17th-century England. In these plays, the cuckold anxiety of earlier periods gives way to cuckold envy:

In A Mad World, My Masters Middleton fully realizes some of the subtle psycho/social details that Jonson develops with the potential cuckold Kitely in Every Man in His Humor. The perverse pleasure that Jonson's acquiescent cuckold derives from his subject position is latent, as Martin Semour-Smith notes, in the etymology of Kitely's name: "Mr. Sale draws attention in his edition to the dialect word 'kittle', meaning 'ticklish' ie. 'hard to deal with, touchy'; but he has missed the verb 'to kittle': 'to stir, with feeling or emotion, usually pleasurable.'" Seymour-Smith continues, noting that it "was also clear to Jonson that Kitely perversely enjoyed his wife less as a direct sexual object than as the indirect object by which he might be cuckolded" (xii, xiii). (Kuchar, 2001, p. 18)

In Every Man in His Humor, the lead character notes the strangeness of his fetish:

Who will not judge him worthy to be robbed,
That sets his doors wide open to a thief,
And shows the felon, where his treasure lies?
(Kuchar, 2001, p. 19)

If 17th-century England is the ground zero for cuckold envy, where was it beforehand? In some yet unknown human population? Or was it in a nonhuman species? Perhaps we are looking at an evolutionary trajectory similar to that of the AIDS virus, i.e., a lengthy period of co-adaptation in a nonhuman population followed by transfer to a human population and increased virulence.

References

Anderson, J.W. (1982). Social structure and the veil: comportment and the composition of interaction in Afghanistan, Anthropos, 77 (3/4), 397.

Belote, L. (1978). Prejudice and pride: Indian-White relations in Saraguro, Ecuador,
Ann Arbor, Michigan: University Microfilms International.

Campbell, J.K. (1964). Honour, family and patronage: a study of institutions and moral values in a Greek mountain community, Oxford: Clarendon Press.

Chagnon, N. (1967). Yanomamö warfare, social organization and marriage alliances,
Ann Arbor, Mich.: University Microfilms.

Cuckold – Wikipedia, http://en.wikipedia.org/wiki/Cuckold

Denaro, F.J., J.L. Lopez-Ribot, and W.L. Chaffin. (1995). Adhesion of Candida albicans to brain tissue of Macaca mulata in an ex vivo assay, Infection and Immunity, 63, 3438-3441.

Evans-Pritchard, E.E. (1937). Witchcraft, oracles and magic among the Azande,
Publisher: Oxford: Clarendon Press.

Gelo, D. (1986). Comanche belief and ritual, Ann Arbor, Mich.: University Microfilms International.

Goldman, I. (1963). The Cubeo: Indians of the Northwest Amazon, Urbana, Illinois: University of Illinois Press.

Kuchar, G. (2001). Rhetoric, Anxiety, and the Pleasures of Cuckoldry in the Drama
of Ben Jonson and Thomas Middleton, Journal of Narrative Theory, 31 (1), Winter, pp. 1-30.

Mormann, K. (2010). Factors influencing parasite-related suppression of mating behavior in the isopod Caecidotea intermedius, Theses and Disserations, paper 48
http://via.library.depaul.edu/etd/48

Schmid, J., P.R. Hunter, G.C. White, A.K. Nand, and R.D. Cannon. (1995). Physiological traits associated with success of Candida albicans strains as commensal colonizers and pathogens, Journal of Clinical Microbiology, 33, 2920–2926.

Schmid, J., M. Rotman, B. Reed, C.L. Pierson, and D.R. Soll. (1993). Genetic similarity of Candida albicans strains from vaginitis patients and their partners, Journal of Clinical Microbiology, 31, 39-46.