Is eye color sex-linked?

Averaged face of blue-eyed male subjects (left). Averaged face of brown-eyed male subjects (right). Czech population. (Kleisner et al., 2010)

If sexual selection of women diversified the eye color of early Europeans, the new colors should tend to be sex-linked, since the selection targeted women more than men. There is now evidence that blue eyes are linked to feminization of face shape.

Throughout most of the world, humans have brown eyes, black hair, and varying shades of dark skin. An exception is Europe, especially its northern and eastern portions. Here, eyes are not only brown but also blue, gray, hazel, or green. Hair is not only black but also brown, flaxen, golden, or red. Finally, skin has been whitened to the end point of depigmentation.

How can we explain this unusual color pattern? Is it simply due to lightening of skin color? In other words, did reduction of skin pigmentation incidentally reduce eye and hair pigmentation? The diverse palette of eye and hair colors would thus be a side effect of selection for lighter skin.

This explanation is dubious. For one thing, the gene loci are not the same. European skin has whitened mainly through allelic change at SLC45A2 (AIM1) and SLC24A5 (Soejima et al., 2005; Voight et al., 2006). European hair has diversified in color through a proliferation of new alleles at MC1R (Makova & Norton, 2005; Rana et al., 1999). European eyes have diversified in color mainly through a proliferation of new alleles at the OCA2-HERC2 gene complex (Duffy et al., 2007; Kayser et al., 2008; Sturm & Frudakis, 2004; Sturm et al., 2008).

Some of these novel hair and eye colors are also associated with lighter skin, notably the red hair and blue eye phenotypes. But why would selection for lighter skin lead to a proliferation of new alleles for hair and eye color—most of which have little or no influence on skin color? Why is it that red hair and blue eyes have not reached fixation in any human population, even those with milk-white skin?

Sexual selection?

I have argued that the cause was an intensification of sexual selection among early Europeans, specifically sexual selection of women (Frost, 2006; Frost, 2008). When too many women have to compete for too few men, there is selection for visible female traits that hyperstimulate certain algorithms in the male brain, particularly those for gender recognition or fertility assessment.

Among hunter-gatherers—and all humans were hunter-gatherers until 10,000 years ago, sexual selection of women tends to intensify farther away from the equator. On the one hand, hunting distances lengthen, thus increasing male mortality. On the other, polygyny becomes less common because women are less able to provide for themselves and their children in winter, thus making it costlier for a man to provide for a second wife. Result: a growing imbalance between the numbers of women and men on the mate market.

Among early modern humans, these two equator-to-arctic trends reached a common end-point in the steppe-tundra of northern Eurasia, such as existed during the last ice age (25,000 – 10,000 years ago). Hunting distances were very long because almost all food came from highly mobile herds of mammals, notably reindeer. Male provisioning was similarly at a maximum, women having little or no food autonomy.

The Eurasian steppe-tundra was continuously inhabited only in portions of its European end, where it ran farther south because of the large icecap over Scandinavia and where the moderating influence of the Atlantic Ocean and the Gulf Stream made the climate moister and milder. Here, the effects of intense sexual selection could accumulate and be passed on from generation to generation. Conversely, northern Asia appears to have suffered episodes of complete depopulation, particularly at the height of the last ice age.

Sexual selection: color novelty and color diversification

When sexual selection is weak, the adaptive equilibrium is dominated by selection for a dull, cryptic appearance that reduces detection by predators (Kirkpatrick, 1987). As sexual selection grows stronger, the equilibrium shifts toward a more noticeable appearance that retains the attention of potential mates, typically by means of vivid and/or novel colors.

One outcome may be a polymorphism of brightly colored phenotypes, due to selection shifting to scarcer and more novel hues whenever a color variant becomes too common (Endler, 1980; Frost, 2006; Hughes et al., 1999; Hughes et al., 2005; Olendorf et al., 2006). This frequency dependence has been shown in humans. Thelen (1983) presented male participants with slides showing attractive brunettes and blondes and asked them to choose, for each series, the woman they would most like to marry. One series had equal numbers of brunettes and blondes, a second 1 brunette for every 5 blondes, and a third 1 brunette for every 11 blondes. Result: the rarer the brunettes were in a series, the likelier any one of them would be chosen.

But why would this stronger selection diversify hair and eye color while simply whitening skin color? The answer seems to be that sexual selection acts on skin color not only through rare-color preference but also by hyperstimulating a gender-recognition algorithm, i.e., by accentuating a visible female-specific trait. In our species, female skin has less melanin and hemoglobin than does male skin, i.e., women look paler, men browner and ruddier (Edwards & Duntley, 1939; Hulse, 1967; Jablonski & Chaplin, 2000).

Sex linkage?

If European skin had whitened through selection for lighter-skinned women, it should have whitened more in women than in men, thus becoming more sexually dimorphic. Yet skin color actually seems to be less dimorphic in Europeans than in other humans (Madrigal & Kelly, 2006). This finding does not necessarily invalidate the sexual selection hypothesis. It may be that the pigmentary sex difference cannot fully express itself in light-skinned populations. Skin color is dimorphic because girls progressively lighten in color during adolescence, and such lightening may be less easily expressed if melanin production is already low. Indeed, this dimorphism seems to be almost absent in people whose skin starts off with very little pigment, such as Dutch and Belgian subjects (Frost, 2007).

And hair and eye color? Sexual selection of women should favor novel hair and eye colors more so in women than in men. Granted, both polymorphisms arose over a short and relatively recent span of time, so sexual selection would have worked with those alleles that were initially available and, for the most part, not sex-linked. But surely a few of these mutant alleles would have been sex-linked and, as such, favored over non-sex-linked ones.

This does seem to be the case with hair color. Blond hair darkens with age more slowly in women than in men (Olivier, 1960, p. 74). A ‘digit ratio’ study indicates that prenatal exposure to estrogen is higher in individuals with blond hair or non-brown eyes (Mather et al., unpublished). The same study, however, found no evidence of sexual dimorphism. Women and men had roughly the same proportions of hair and eye colors among the 18-to-38 year olds under study. Such a dimorphism, if it does exist, may be a transient one limited to younger age groups.

Moreover, Kleisner et al. (2010) have found an apparent sex linkage between blue eyes and feminization of face shape. They initially wished to determine whether eye color influences perception of male dominance, using facial pictures of Czech men. The results showed that brown-eyed men were rated as more dominant than blue-eyed men. As a control, the authors repeated the experiment after altering the facial photos of the brown-eyed men to make them blue-eyed. These altered photos were still rated as more dominant.

Careful study of the photos revealed that the brown-eyed men had more masculine facial features:

In contrast with blue-eyed males, brown-eyed males have statistically broader and rather massive chins, broader (laterally prolonged) mouths, larger noses, and eyes that are closer together with larger eyebrows. In contrast, blue-eyed males show smaller and sharper chins, mouths that are laterally narrower, noses smaller, and a greater span between the eyes.

The perception of brown-eyed men as more dominant is thus due to their more masculine facial appearance—and not to their brown eyes. The authors suggest that some kind of sex linkage may be responsible, while adding: “Repeating this study in other populations with polymorphism in eye color can test this hypothesis.”

If true, this finding would be consistent with Liberton et al. (2009) who found that European face shape has differentiated from West African face shape through a selective force that has acted primarily on women. Both findings, in turn, would support my argument that many of the differences we see among human populations are not due to differences in natural selection, and hence differing natural environments. Instead, the cause lies in differing intensities of sexual selection, and whether this selection has primarily targeted men or women (Frost, 2008).

When men are the prime targets of sexual selection, as in tropical ‘female farming’ societies, the result is accentuation of certain male features. Meanwhile, there is a slackening of female-targeted sexual selection, which leads to women having a more functional and less ornamental appearance. This pattern is reversed when women are the prime targets of sexual selection (Frost, 2008).

Ethnic substructure?

There is admittedly an alternate explanation for the above finding: ethnic substructure among the Czech subjects. The Czech Republic has historically been home to ethnic minorities who statistically differ from ethnic Czechs in facial appearance, i.e., Jews, Germans, and Roma. Jews and Roma, like other populations of Mediterranean or southwest Asian origin, tend to have brown eyes and a more robust face shape. Conversely, Germans are likelier to have blue eyes and more gracile faces. Although the Jewish and German communities were severely decimated during World War II and its aftermath, with many survivors later emigrating, there still remain significant numbers of Czech citizens who are wholly or partly of Jewish or German origin. Since WWII, there has also been an influx of Roma into the Czech Republic.

It would be difficult to rule out this kind of explanation, even if one questioned the subjects of the study. After the last war, many Czech citizens of Jewish or German origin felt it best to conceal their ancestry, for fear of discrimination or even expulsion from the country. Today, their grandchildren may be completely unaware of their origins.

This is all the more reason to replicate the results with subjects from another population, preferably one with as little ethnic substructure as possible.

References

Duffy, D.L., G.W. Montgomery, W. Chen, Z.Z. Zhao, L. Le, M.R. James, N.K. Hayward, N.G. Martin, & R.A. Sturm. (2007). A three-single-nucleotide polymorphism haplotype in intron 1 of OCA2 explains most human eye-color variation. American Journal of Human Genetics, 80, 241-52.

Edwards, E.A., & S.Q. Duntley. (1939). The pigments and color of living human skin. American Journal of Anatomy, 65, 1-33.

Endler, J.A. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution, 34, 76‑91.

Frost, P. (2008). Sexual selection and human geographic variation, Special Issue: Proceedings of the 2nd Annual Meeting of the NorthEastern Evolutionary Psychology Society. Journal of Social, Evolutionary, and Cultural Psychology, 2(4),169-191.

http://www.jsecjournal.com/articles/volume2/issue4/NEEPSfrost.pdf

Frost, P. (2007). Comment on Human skin-color sexual dimorphism: A test of the sexual selection hypothesis, American Journal of Physical Anthropology, 133, 779-781.

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior, 27, 85-103.

Hughes, K.A., L. Du, F.H. Rodd, & D.N. Reznick. (1999). Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Animal Behaviour, 58, 907-916.

Hughes, K.A., F.H. Rodd, & D.N. Reznick. (2005). Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). Journal of Evolutionary Biology, 18, 35-45.

Hulse, F.S. (1967). Selection for skin color among the Japanese. American Journal of Physical Anthropology, 27, 143-156.

Jablonski, N.G., & G. Chaplin. (2000). The evolution of human skin coloration. Journal of Human Evolution, 39, 57-106.

Kayser, M., F. Liu, A.C.J.W. Janssens, F. Rivadeneira, O. Lao, K. van Duijn, M. Vermeulen, P. Arp, M.M. Jhamai, W.F.J. van Ijcken, J.T. den Dunnen, S. Heath, D. Zelenika, D.D.G. Despriet, C.C.W. Klaver, J.R. Vingerling, P.T.V.M. de Jong, A. Hofman, Y.S. Aulchenko, A.G. Uitterlinden, B.A. Oostra, & C.M. van Duijn. (2008). Three genome-wide association studies and a linkage analysis identify HERC2 as a human iris color gene. The American Journal of Human Genetics doi:10.1016/j.ajhg.2007.10.003

Kirkpatrick, M. (1987). Sexual selection by female choice in polygynous animals. Annual Review of Ecology and Systematics, 18, 43-70.

Kleisner, K., T. Kočnar, A. Rubešova, and J. Flegr. (2010). Eye color predicts but does not directly influence perceived dominance in men, Personality and Individual Differences, 49, 59–64.

Liberton, D.K., K.A. Matthes, R. Pereira, T. Frudakis, D.A. Puts, & M.D. Shriver. (2009). Patterns of correlation between genetic ancestry and facial features suggest selection on females is driving differentiation. Poster #326, The American Society of Human Genetics, 59th annual meeting, October 20-24, 2009. Honolulu, Hawaii.

Mather, F., J.T. Manning, & P.E. Bundred. (unpublished). 2nd to 4th digit ratio, hair and eye colour in Caucasians: Evidence for blond hair as a correlate of high prenatal oestrogen.

Makova, K, & H. Norton. (2005). Worldwide polymorphism at the MC1R locus and normal pigmentation variation in humans. Peptides, 26, 1901-1908.

Olendorf, R., F.H. Rodd, D. Punzalan, A.E. Houde, C. Hurt, D.N. Reznick, & K.A. Hughes. (2006). Frequency-dependent survival in natural guppy populations. Nature, 44, 633-636.

Olivier, G. (1960). Pratique anthropologique. Paris: Vigot Frères.

Rana, B.K., D. Hewett‑Emmett, L. Jin, B.H.-J. Chang, N. Sambuughin, M. Lin, S. Watkins, M. Bamshad, L.B. Jorde, M. Ramsay, T. Jenkins, & W-H. Li. (1999). High polymorphism at the human melanocortin 1 receptor locus. Genetics, 151, 1547‑1557.

Soejima, M., H. Tachida, T. Ishida, A. Sano, & Y. Koda. (2005). Evidence for recent positive selection at the human AIM1 locus in a European population. Molecular Biology and Evolution, 23, 179-188.

Sturm, R.A., D.L. Duffy, Z.Z. Zhao, F.P.N. Leite, M.S. Stark, N.K. Hayward, N.G. Martin, & G.W. Montgomery. (2008). A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue-brown eye color. The American Journal of Human Genetics, 82, 424-431.

Sturm, R.A., & T.N. Frudakis. (2004). Eye colour: portals into pigmentation genes and ancestry. Trends in Genetics, 20, 327-332.

Thelen, T.H. (1983). Minority type human mate preference. Social Biology, 30, 162-180.

Voight, B.F., S. Kudaravalli, X. Wen, & J.K. Pritchard. (2006). A map of recent positive selection in the human genome. PLoS Biology, 4(3), e72 doi:10.1371/journal.pbio.0040072

The demon within. Part III

Sir John Hawkins (1532-1595) was instrumental in bringing England into the slave trade. Was this trade a source of new pathogens for the English population?

Some vaginal strains of Candida albicans have become better at sexual transmission, such as through improved adhesion to saliva-coated surfaces and through displacement of non-vaginal strains in a new host.

But the adaptations don’t stop there. In my last two posts, I argued that these strains have also become better at sexual transmission by manipulating host behavior. They can cross the blood/brain barrier. We know this. Once inside the control room, why not go one step farther?

C. albicans is an ideal candidate for such evolution. First, It’s common. There’s a large pool of genetic variants for natural selection to act upon.

Second, C. albicans has developed the capacity to spread from one host to another through intimate contact. It thus has every reason to enhance this capacity by rewiring its host’s neural circuits, even at the cost of doing much harm.

As biologist Paul Ewald observed:

For decades medical science was dominated by the doctrine of "commensalisms' - the notion that the pathogen-host relationship inevitably evolves toward peaceful coexistence, and the pathogen itself toward mildness, because it is in the germ's interest to keep its host alive. This sounds plausible, but it happens to be wrong.

[…] If you're a germ that can travel from person to person by way of a "vector," or carrier, such as a mosquito or a tsetse fly, you can afford to become very harmful. This is why, Ewald argues, insect borne diseases such as yellow fever, malaria, and sleeping sickness get so ugly. Cholera uses another kind of vector for transmission: it is generally waterborne, travelling easily by way of faecal matter shed into the water supply. And it, too, is very ugly. (Hooper, 1999)

An infectious organism will thus try to turn its host into a launching pad for infection of other hosts. The long-term survival of any one host no longer matters.

Avenues for future enquiry

Where from?

If a pathogen is responsible for cuckold envy, and if the first recorded mention of this fetish comes from 17th-century England, the point of origin is probably extra-European. Specifically, it would have been a society that came into contact with England through that country’s expansion of foreign trade, exploration, and colonization from the 16th century onward. We’re probably looking at the West Indies, West Africa, the eastern American seaboard, or the territories of the Hudson’s Bay Company.

One of my commenters, Jim Bowery, suggested that the pathogen could have entered England via the West African slave trade. Indeed, an argument can be made that sexually transmitted diseases are most likely to develop in high-polygny societies, such as exist among the ‘female-farming’ peoples of sub-Saharan Africa. On the one hand, the polygynous male cannot sexually satisfy all of his wives. On the other, many young males are locked out of the marriage market, the result being a lot of sex on the sly.

As anthropologist Pierre van den Berghe pointed out:

The temporary celibacy of young men in polygynous societies is rarely absolute, however. While it often postpones the establishment of a stable pair-bond and the procreation of children, it often does not preclude dalliance with unmarried girls, adultery with younger wives of older men, or the rape or seduction of women conquered in warfare. Thus, what sometimes looks like temporary celibacy is, in fact, temporary promiscuity. (van den Berghe, 1979, pp. 50-51).

Do other STDs manipulate human sexual behavior?

Is manipulation of sexual behavior a logical adaptation for STDs? If so, have other human STDs evolved in this direction? No one seems to have asked the question. Admittedly, cause and effect are hard to tease apart. Do STDs correlate with sexual promiscuity solely because a promiscuous person is more likely to catch one? Which is the chicken and which is the egg?

Research on insects has turned up several cases of an STD manipulating host behavior in order to facilitate sexual transmission.

Behavioural changes associated with parasitic infection are well known, and at least some of these appear to be adaptations on the part of the parasite to increase transmission (Moore, 1993, 2001; Poulin, 1994a, b, 1998a, 2000). Four recent studies of insect STDs are relevant here. McLachlan (1999) showed that male midges (Paratrichocladius rufiventris) infected with the mite Unionicola ypsilophora were more likely to be in mating pairs than uninfected males. As discussed earlier, the mites rely on female midges to return them to water to complete their life cycle. If they find themselves on a male midge, therefore, they are effectively dead unless their host mates with a female […].

Raina et al. (2000) found that Hz-2V infected female corn earworm moths Helicoverpa zea produce two to three times more sex pheromone than uninfected female moths, possibly enhancing their ability to attract male moths, although they also reported that these animals vigourously resisted mating. Abbot & Dill (2001) found that male Labidomera clivicollis beetles infected with the mite Chrysomelobia labidomera were more likely to displace other males from mating pairs, which again could be interpreted as being adaptive manipulation of the host by the parasite to increase transmission. Webberley et al. (2002), by contrast, found that infection of Adalia bipunctata with Coccipolipus hippodamiae did not have any effect on the mating behaviour of the host. (Knell & Webberley, 2004)

References

Hooper, J. (1999). A new germ theory, The Atlantic Journal, February

http://gc.homeunix.net/

Knell, R.J., and K.M. Webberley. (2004). Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour, Biol. Rev., 79, 557–581.

van den Berghe, P.L. (1979). Human Family Systems. An Evolutionary View, New York: Elsevier.

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.

The demon within

Candida albicans. Some strains have adapted to sexual transmission. Have they gone so far as to manipulate host behavior?

Vulvovaginal candidiasis (VVC), commonly known as vaginal yeast infection, affects 70-75% of sexually active women at least once and 5-8% recurrently (Li et al., 2008). It is usually caused by Candida albicans, a single-celled fungus that reproduces asexually.

Although C. albicans can colonize many body sites, some strains have specifically adapted to the vagina. This evolutionary trajectory seems to have gone through three levels of adaptation:

Adaptation to vaginal environments

Vaginally adapted strains are a small subset of C. albicans. In China, two strains account for almost 60% of all VVC cases, yet neither is present at extragenital sites (Li et al., 2008). In the United States, C. albicans strains are much more diverse in the male partners of women without VVC than in the vaginas of women with or without VVC (Schmid et al., 1993).

Adaptation to sexual transmission

These vaginal strains seem to have also adapted to sexual transmission, specifically female-to-male transmission. Once VVC develops, they can spread to the host’s male partner by colonizing his glans penis via vaginal intercourse (Li et al., 2008) or his oral cavity via cunnilingus (Schmid et al., 1995). Vagina-to-vagina transmission has also been attested in lesbian couples (Bailey et al., 2008).

There is evidence of genetic changes for sexual transmissibility. Vaginal strains 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 of C. albicans (Schmid et al., 1993).

Adaptation to certain sexual behaviors

Although a relationship clearly exists between sexual behavior and VVC, it is not a simple one of cause and effect. This is the conclusion of two research teams, Hellberg et al. (1995) and Reed et al. (2003), who sought to identify those aspects of sexual behavior that correlate with VVC.

Hellberg et al. (1995) found no significant association between VVC and the main indicators of vaginal sexual activity: (1) frequency of vaginal sex; (2) history of multiple sexual partners (more than 10 lifetime partners); and (3) sex with more than one partner during the last six months.

There were, however, significant associations with (1) early age of first intercourse, (2) casual sex with previous unknown partners in the past month, (3) vaginal sex during menstruation, (4) oral sex (fellatio), and (5) receptive anal sex.

Reed et al. (2003) reported similar findings. VVC was not significantly associated with frequency of vaginal sex, lifetime number of partners, and duration of current relationship. But there were significant associations with cunnilingus in the past month and masturbation in the past month. Unlike Hellberg et al. (1995), there were no significant associations with early age of first intercourse or frequency of receptive anal sex.

Reed et al. (2003) also found two risk factors in the male partner: early age of first intercourse and masturbation in the past month. There were no significant associations with his marital status, lifetime number of partners, previous partners with VVC, personal history of yeast infections, or reported fellatio or cunnilingus in the past month.

This is all rather puzzling. Occurrence of VVC was related not to vaginal sex but rather to non-vaginal sex, i.e., fellatio, cunnilingus, and masturbation. Even more puzzling, Reed et al. (2003) failed to find any association between VVC and the presence of C. albicans in the male partner, including his oral cavity. The authors concluded that the relationship between VVC and sexual behavior is not primarily one of sexual transmission:

If the association between orogenital contact and recurrent Candida vulvovaginitis is not mediated by transmission of the organism, how might increased risk be conferred? Previous study of the immunopathogenesis of recurrent Candida vulvovaginitis suggests that a delicate equilibrium exists among C. albicans, vaginal bacterial flora, and vaginal defense mechanisms, and that changes in the host environment promote the transformation of C. albicans from a saprophytic to a pathogenic existence. We suggest that the effects of genital washing with saliva—from either the male or the female—might upset this balance […] (Reed et al., 2003)

But how would this vaginal equilibrium be upset by the woman fellating her male partner? And how would it be upset by her male partner masturbating—alone and by himself?

Manipulation of host behavior?

To make sense of all this, we should perhaps reverse the direction of causality. Perhaps some vaginal strains of C. albicans have reached a third level of adaptation, i.e., manipulation of host behavior to increase opportunities for sexual transmission. Perhaps they somehow weaken the host’s sexual inhibitions and incite her to maximize contact between her vaginal fluids and colonizable sites on her partner’s body.

Does this sound like science fiction? Keep in mind that parasites manipulate host behavior in many non-human animals, and some of these parasites are likewise fungi (see here). Moreover, C. albicans has evolved the ability to cross the blood-brain barrier and colonize sites in the human brain (Jong et al., 2001). According to an autopsy of macaque brains, this microbe can recognize different kinds of neural tissue:

An ex vivo adhesion assay was used to examine adhesion of Candida albicans yeast cells to brain tissue of the primate Macaca mulata. Tissues from frontal lobes and striatum (caudate, putamen, and portions of the globus pallidus) were used in the assay. Yeast cells adhered to gray matter at about six times the level of adhesion to white matter. The fungus was able to bind to different cell types within the cortex, basal ganglia, and white matter. (Denaro et al., 1995)

One can imagine a multi-stage process of development:

1. “Behavior-modifying” C. albicans colonizes the vagina as a commensal organism with low virulence and no VVC. The ensuing period of latency might last a long time.

2. Meanwhile, the microbe spreads to other sites within the host’s body, including certain areas of the brain that influence sexual behavior.

3. Once this secondary colonization is complete, the area of primary colonization enters a highly infectious stage, i.e., VVC. The microbe is now ready to spread to her sexual partner.

And how will it influence her partner’s behavior? We cannot find the answer by studying his behavior before and during VVC—as in current studies. We must examine his subsequent behavior, i.e., once this strain of C. albicans has spread to his body and replaced other strains. Are there any behavioral changes?

But, then, what sort of changes should we expect?

(to be cont’d)

References

Bailey, J.V., R. Benato, C. Owen, and J. Kavanagh. (2008). Vulvovaginal candidiasis in women who have sex with women, Sexually Transmitted Diseases, 35, 533–536

Brainwashed by a parasite, Neurophilosophy, August 9, 2007
http://scienceblogs.com/neurophilosophy/2007/08/brainwashed_by_a_parasite.php

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

Hellberg, D., B. Zdolsek, S. Nilsson, and P-A. Mårdh. (1995). Sexual behavior of women with repeated episodes of vulvovaginal Candidiasis, European Journal of Epidemiology, 1, 575-579, 1995

Jong, A.Y., M.F. Stins, S-H. Huang, S.H.M. Chen, K.S. Kim. (2001). Traversal of Candida albicans across human blood-brain barrier in vitro, Infection and Immunity, 69, 4536-4544.

Li, J., S-R. Fan, X-P. Liu, D-M Li, Z-H. Nie, F. Li, H. Lin, W-M. Huang, L-L. Zong, J-G. Jin, H. Lei, and F-Y. Bai. (2008). Biased genotype distributions of Candida albicans strains associated with vulvovaginal candidosis and candidal balanoposthitis in China, Clinical Infectious Diseases, 47, 1119–25.

Reed, B.D., P. Zazove, C.L. Pierson, D.W. Gorenflo, and J. Horrocks. (2003). Candida transmission and sexual behaviors as risks for a repeat episode of Candida vulvovaginitis, Journal Of Women’s Health, 12, 979-989.

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.