In my last column, I reviewed the findings of Butovskaya et al. (2015) on testosterone and polygyny in two East African peoples:
- Testosterone levels were higher in the polygynous Datoga than in the monogamous Hadza. This difference is innate.
- Datoga men were more aggressive than Hadza men on all measures used (physical aggression, verbal aggression, anger, and hostility)
- Datoga men were larger and more robust than Hadza men
- All of these characteristics seem to be adaptive under conditions when men have to compete against other men for access to women
Testosterone levels were not only higher in the Datoga but also more variable. Alvergne et al. (2009) studied this variability in Senegalese men, finding that the monogamous ones differed from the polygynous ones in the way testosterone levels changed with age. The levels were higher in the polygynous men than in the monogamous men between the ages of 15 and 30. After 45, this pattern reversed: the monogamous men had the higher levels. At all ages, the polygynous men were more extraverted than the monogamous ones, this quality being defined as “pro-social behavior which reflects sociability, assertiveness, activity, dominance and positive emotions.” Extraversion may assist a reproductive strategy of seducing women, rather than providing for them.
Thus, when Africans gave up hunting and gathering for farming, there was selection for a new package of male traits. Some of these traits are physiological (higher testosterone levels), some anatomical (denser bones, greater arm and leg girth; changes to muscle fiber properties, etc.), and some behavioral (polygyny, aggressiveness, extraversion, etc.). But this selection didn’t eliminate older genotypes, at least not wholly. There seems to be a balanced polymorphism that allows a minority of quieter, monogamous men to thrive in a high-polygyny society like Senegal. When polygynous men become too numerous, they may spend too much time looking for mating opportunities and not enough checking up on their current wives to avoid being cuckolded. It might be better for some to live continuously with one wife.
African Americans versus Euro Americans
The above differences within sub-Saharan Africa (Datoga vs. Hadza, polygynous Senegalese vs. monogamous Senegalese) are also seen between African Americans and Euro Americans. In all these cases, the differences are of degree and proportion, rather than absolute and non-overlapping.
Testosterone reaches high levels in young African American adults (Pettaway, 1999; Ross et al., 1986; Ross et al., 1992; Winters et al., 2001). African Americans are also likelier to have alleles for high androgen-receptor activity (Kittles et al.,2001). Lifetime exposure to testosterone is reflected in development of prostate cancer, with African American men having the world’s highest incidences (Brawley and Kramer, 1996). It was once thought that lower incidences prevail among black West Indians and sub-Saharan Africans, but underreporting is now thought to be responsible (Glover et al., 1998; Ogunbiyi and Shittu, 1999;Osegbe, 1997).
In African Americans, blood testosterone levels peak during adolescence and early adulthood, being higher than those of Euro Americans of the same age. Levels decline after 24 years of age, and by the early 30s are similar to those of European Americans (Gapstur et al., 2002; Nyborg, 1994, pp. 111-113; Ross et al., 1986; Ross et al., 1992; Tsai et al., 2006; Winters et al., 2001). This is the same pattern we saw in polygynous Senegalese men versus monogamous Senegalese men. In short, polygyny seems associated with a more exaggerated pattern of variation with age.
The demographic contradictions of a high-polygyny society
Testosterone levels are normally higher in all young men, but why are they higher still when polygyny is common? The reason seems to be the scarcity of available women. High-polygyny societies generate a shortage of mateable women, and this shortage is managed by giving priority to men who are at least ten years past puberty. For instance, among the Nyakyusa: “[...] there is a difference of ten years or more in the average marriage-age of girls and men, and it is this differential marriage-age which makes polygyny possible” (Wilson, 1950, p. 112).
By concentrating celibacy among young men, this age rule compels them to seek sex through warfare or illicit means. According to Pierre van den Berghe (1979, pp. 50-51):
Typically, the more men are polygynous in a given society, the greater the age difference between husbands and wives. [...] 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. These young men often devote themselves to warfare during their unmarried years and sometimes homosexuality is tolerated during that period.
For young men in a high-polygyny society, warfare—typically raids against neighboring communities—is the main way to gain access to women. In a sense, war becomes a means of resolving the demographic contradictions of a high-polygyny society. Polygyny creates a wife shortage among young men, and this contradiction is resolved by turning it outward. As warriors, young men are encouraged to satisfy their sexual urges through raids against neighboring peoples. Warfare thus becomes endemic.
This relationship between polygyny and war has often been noted in studies of African societies:
Dorjahn (1959) says African warfare emphasized taking captives, rather than killing the enemy. Kelly’s discussion of Nuer warfare provides an interesting perspective on this phenomenon. In Nuer warfare the main casualties were younger men and older women, with male and female mortality being almost equal. Younger women and children were captured. Female captives were valued because they could be used to generate bridewealth when they were married to other Nuer, whereas captive boys were adopted into the lineage of their captor and would require bridewealth payment when they married. Consequently, few males were taken captive (Kelly 1985:56-57). (White and Burton, 1988)
In their cross-cultural study of the causes of polygyny, White and Burton (1988) conclude that “polygyny is associated with warfare for plunder and/or female captives”:
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[...] polygyny is seen as associated with the expansion of male-oriented kin groups through favorable environments, facilitated by capture of women or bridewealth via warfare. Following this analysis, it is difficult to see polygyny as having benign effects upon the lives of all women. Rather, polygyny produces benefits for senior wives, who have sons and can mobilize the labor of junior wives and children (Hartung 1982); it has negative effects on women who become slaves, captives, or junior wives, or who do not have sons.
We now come to a leading cause of the African slave trade. Polygyny led to warfare, which led to a surplus of unwanted male captives. These captives could be sold as slaves, but local markets would soon be saturated. The excess supply had to be sold farther away, with the result that slave trading networks began to reach the Middle East as early as the time of Christ (Frost, 2008).
While outsiders from the Middle East and Europe would later get more and more involved, becoming not only traders but also captors, it was Africans themselves who initially controlled the supply chain. In its early stages, and even later, this trade was driven by factors internal to Africa.
Whenever I discuss this subject, some people will counter that certain studies have shown an absence of racial/ethnic differences in testosterone levels. Let me discuss these studies at some length.
This meta-analysis concluded: “After adjustment for age, black men have a modestly but significantly 2.5 to 4.9% higher free testosterone level than white men.” Here, “adjustment for age” means comparing black and white men of the same age. The conclusion isn’t surprising, since African American men have a testosterone advantage only from puberty to their early 30s. At other ages, their testosterone levels are either equal to or less than those of Euro American men.
This meta-analysis has two other flaws. First, it included only studies on “men,” thus excluding studies on teenagers, among whom the race difference is greatest.
Second, it included Rohrmann et al. (2007). This study suffers from serious methodological problems, as I will now explain.
This study concluded that “contrary to the postulated racial difference, testosterone concentrations did not differ notably between black and white men.”
This study also found that 45-69 year old black men have higher testosterone levels (5.62 ng/ml) than do 20-44 year old black men (5.35 ng/ml). Such a finding is paradoxical and indicates a faulty dataset. The authors used serum samples from the National Center for Health Statistics that had been earlier collected for its Third National Health and Nutrition Examination Survey (NHANES III). The authors state they used 1,479 samples that remained out of an initial total of 1,998. Over 25% of the original samples were missing. The authors state that some samples were missing because they were being used for another study.
The same serum bank had in fact been used for research on a sexually transmitted disease. This was the study by Fleming et al. (1997), who reported that more than 25% of adults between 30 and 39 years of age were positive for HSV-2 (Herpes Simplex virus type 2). Those samples may have been set aside either for further testing or for legal reasons. The serum bank would have thus lost some of its most polygynous donors.
This study measured salivary testosterone in young men (15-30 years) from the United States, Congo, Nepal, and Paraguay. Americans had the highest levels (335 pmol/l), followed by Congolese (286 pmol/l), Nepalese (251 pmol/l), and Paraguayans (197 pmol/l).
Who were these Americans? They are simply identified as … young Americans—a demographic that is now less than 60% of European descent. In Boston, where the study was conducted, public schools in 2005 were 46% black and 31% Latino (mainly Puerto Ricans and Dominicans). The authors also state that “the USA participants were recruited by public advertisement.” The pool of participants may have therefore resembled that of people who give blood in exchange for payment, i.e., it may have been disproportionately poor and non-white. In any event, the results are unusable without any information on racial background.
The Congolese participants were likewise unrepresentative of Congolese in general. They were Lese who inhabit the Ituri forest in proximity to the Efe pygmies. Many Lese are, in fact, partly of pygmy ancestry. As such, their testosterone levels would be closer to that of hunter-gatherers with lowers levels of polygyny and less male-male competition for mates.
This study concluded that testosterone levels did not differ between African American and Euro American boys between the ages of 6 and 18. Such a finding is to be expected for the first few years of this age range, when no difference should exist between the two groups. The main flaw, however, is that the participants were compared not by age but by Tanner stage. Since African Americans enter puberty earlier, this study compared younger African American boys with older Euro American boys.
Testosterone levels may differ between the two groups because of earlier maturation by African American boys. But why would this difference persist beyond adolescence and into the mid-twenties? This question remains unresolved because none of the participants were older than 18.
Various African studies
Several studies have found lower testosterone levels in African populations than in North Americans. This difference might be partly due to the effects of malnutrition or infectious diseases, notably among the Zimbabwean subjects studied by Lukas et al. (2004). The main reason, however, is that these studies mostly had middle-aged or even elderly participants. Lukas et al. (2004) report a mean age of 42.18. The scatter plot (Fig. 2) suggests a logarithmic decline in testosterone with age, but there were too few participants below 25 for analysis of that age group. The same criticism applies to Campbell et al. (2003), a study of testosterone levels in Ariaal pastoralists from northern Kenya. The mean age was 46.8.
In addition, some of these studies concern hunter-gatherers, like the !Kung of Namibia and the Ituri Forest pygmies of the Congo, who have low polygyny rates and weak male-male competition for mates (e.g., Winkler and Christiansen, 1993). Their low testosterone levels are thus to be expected.
Alvergne, A., M. Jokela, C. Faurie, and V. Lummaa. (2010). Personality and testosterone in men from a high-fertility population,Personality and Individual Differences, 49, 840-844.
Alvergne, A., M. Jokela, and V. Lummaa. (2010). Personality and reproductive success in a high-fertility human population,Proceedings of the National Academy of Sciences, 107, 11745-11750.
Alvergne, A., C. Faurie, and M. Raymond. (2009). Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population, Hormones and Behavior, 56, 491-497.
Brawley, O.W. and B.S. Kramer. (1996). Epidemiology of prostate cancer. In N.J. Volgelsang, P.T. Scardino, W.U. Shipley, and D.S. Coffey. (eds). Comprehensive textbook of genitourinary oncology. Baltimore: Williams and Wilkins.
Butovskaya M.L., O.E. Lazebny, V.A. Vasilyev, D.A. Dronova, D.V. Karelin, A.Z.P. Mabulla, et al. (2015). Androgen receptor gene polymorphism, aggression, and reproduction in Tanzanian foragers and pastoralists. PLoS ONE 10(8): e0136208.
Campbell, B., O’Rourke, M.T., and Lipson, S.F. (2003). Salivary testosterone and body composition among Ariaal males, American Journal of Human Biology, 15, 697-708.
Ellison, P.T., Bribiescas, R.G., Bentley, G.R., Campbell, B.C., Lipson, S.F., Panter-Brick, C., and Hill, K. (2002). Population variation in age-related decline in male salivary testosterone.Human Reproduction, 17, 3251-3253.
Fleming D.T., G.M. McQuillan, R.E. Johnson, A.J. Nahmias, S.O. Aral, F.K. Lee, and M.E. St Louis. (1997). Herpes simplex virus type 2 in the United States, 1976 to 1994, New England Journal of Medicine, 337, 1105-11.
Frost, P. (2008). The beginnings of black slavery, Evo and Proud, January 25
Gapstur, S.M., P.H. Gann, P. Kopp, L. Colangelo, C. Longcope, and K. Liu. (2002). Serum androgen concentrations in young men: A longitudinal analysis of associations with age, obesity, and race. The CARDIA male hormone study, Cancer Epidemiology, Biomarkers & Prevention, 11, 1041-1047.
Glover, F.E. Jr., D.S. Coffey, L.L. Douglas, M. Cadogan, H. Russell, T. Tulloch, T.D. Baker, R.L. Wan, and P.C. Walsh. (1998).The epidemiology of prostate cancer in Jamaica, Journal of Urology, 159, 1984-1986.
Kittles, R.A., Young, D., Weinrich, S., Hudson, J., Argyropoulos, G., Ukoli, F., Adams-Campbell, L. and Dunston, G.M. (2001). Extent of linkage disequilibrium between the androgen receptor gene CAG and GGC repeats in human populations: implications for prostate cancer risk, Human Genetics, 109, 253-261.
Lukas, W.D., B.C. Campbell, and P.T. Ellison. (2004). Testosterone, aging, and body composition in men from Harare, Zimbabwe, American Journal of Human Biology, 16, 704-712.
Nyborg, H. (1994). Hormones, Sex, and Society. The Science of Physiology. Westport (Conn.): Praeger.
Ogunbiyi, J. and O. Shittu. (1999). Increased incidence of prostate cancer in Nigerians. Journal of the National Medical Association, 3, 159-164.
Osegbe, D.N. (1997). Prostate cancer in Nigerians: facts and non-facts, Journal of Urology, 157, 1340-1343.
Pettaway, C.A. 1999. Racial differences in the androgen/androgen receptor pathway in prostate cancer, Journal of the National Medical Association, 91, 653-660.
Richard, A., S. Rohrmann, L. Zhang, M. Eichholzer, S. Basaria, E. Selvin, A.S. Dobs, N. Kanarek, A. Menke, W.G. Nelson, and E.A. Platz. (2014). Racial variation in sex steroid hormone concentration in black and white men: a meta-analysis, Andrology, 2(3), 428-35
Richards, R.J., F. Svec, W. Bao, S.R. Srinivasan, and G.S. Berenson. (1992). Steroid hormones during puberty: racial (black-white) differences in androstrenedione and estradiol. The Bogalusa heart study, The Journal of Clinical Endocrinology & Metabolism,75, 624-631.
Rohrmann, S., Nelson, W.G., Rifai, N., Brown, T.R., Dobs, A., Kanarek, N., Yager, J.D., Platz, E.A. (2007). Serum estrogen, but not testosterone levels differ between Black and White men in a nationally representative sample of Americans, The Journal of Clinical Endocrinology & Metabolism, 92, 2519-2525
Ross, R.K., Bernstein, L., Lobo, R.A., Shimizu, H., Stanczyk, F.Z., Pike, M.C. and Henderson, B.E. (1992). 5-apha-reductase activity and risk of prostate cancer among Japanese and US white and black males, Lancet, 339, 887-889.
Ross, R., Bernstein, L., Judd, H., Hanisch, R., Pike, M., & Henderson, B. (1986). Serum testosterone levels in healthy young black and white men, Journal of the National Cancer Institute, 76, 45-48.
Tsai, C.J., B.A. Cohn, P.M. Cirillo, D. Feldman, F.Z. Stanczyk, A.S. Whittemore. (2006). Sex steroid hormones in young manhood and the risk of subsequent prostate cancer: a longitudinal study in African-Americans and Caucasians (United States), Cancer Causes Control, 17, 1237-1244.
van den Berghe, P.L. (1979). Human Family Systems. An Evolutionary View. New York: Elsevier.
White, D.R., and M.L. Burton. (1988). Causes of polygyny: ecology, economy, kinship, and warfare, American Anthropologist,90, 871-887.
Wilson, M. (1950). Nyakyusa kinship. In Radcliffe-Brown, A.R., & Forde, D. (eds). African Systems of Kinship and Marriage, pp. 111-139, London: Oxford University Press.
Winkler, E-M., and Christiansen, K. (1993). Sex hormone levels and body hair growth in !Kung San and Kavango men from Namibia. American Journal of Physical Anthropology, 92, 155-164.
Winters, S.J., Brufsky, A., Weissfeld, J., Trump, D.L., Dyky, M.A. & Hadeed, V. (2001). Testosterone, sex hormone-binding globulin, and body composition in young adult African American and Caucasian men, Metabolism, 50, 1242-1247.