Monday, August 6, 2018

Why is IQ declining in the Arab world?



African migrants at the Egyptian-Israeli border (Wikicommons)



During most of the twentieth century people did better and better on IQ tests. This increase, dubbed the Flynn effect, is now plateauing in the Western world. It is even reversing in Scandinavia and France (Bratsberg and Rogeberg 2018; Dutton and Lynn 2015; Flynn 2007, p. 143; Teasdale and Own 2005).

A similar plateauing and even reversal has begun in the Arab world. In Kuwait, mean IQ fell an average of 6.2 points between 2006 and 2015 (Dutton et al. 2017a). In Damascus, it remained unchanged between 2004 and 2013/14 (Dutton et al. 2018a). In Khartoum, it fell an average of 2.13 points between 1999 and 2010 (Dutton et al. 2017b).


Khartoum: is the Flynn effect continuing?

The authors of the Khartoum study later retracted their finding, however. Because the earliest data had been collected just before the introduction of compulsory schooling in 1999, the IQ decline could simply reflect a change in sampling: from middle-class children to children in general. There were also strange age differences: IQ scores declined in some age groups but not in others. So the authors conducted a second study, examining only data from students with a compulsory schooling background. They now found an increase in mean IQ from 2004 to 2016, i.e., a positive Flynn effect (Dutton et al. 2018b).

On the other hand, “compulsory schooling background" may also mean a different ethnic background. When I enquired about this point, Dr. Bakhiet replied that the study was done in residential areas of Khartoum where there were no refugees or immigrants. The participants thus “represent the people of northern Sudan” and were not recruited from among the millions of migrants who live on the city’s outskirts.

As for the first Khartoum study, we know little about the ethnic background of the participants. Some of them seem to have had migrant backgrounds. We should keep in mind that many refugees were initially housed within the city limits and that not all migrants ended up in refugee facilities. Unfortunately, it would be difficult to find out more because the lead researcher, Dr. Omar Khaleefa, was abducted and apparently murdered in 2012. I suspect that this kind of information was not recorded at the time, given the delicate nature of ethnic identity in Sudan.

In sum, the second Khartoum study largely excludes the city’s immigrant population, and it is this study that provides a reassuring picture of rising IQ. As for the first Khartoum study, we know less about the ethnic makeup of its participants, particularly whether their ethnic makeup changed over time. This is an important factor to consider. Khartoum is now overwhelmingly a city of migrants from the south, and it is unlikely that many will ever return home.


Possible causes 

Why this apparent plateauing or reversal in places as different as Khartoum, Kuwait, and Damascus? The authors cite several possible causes:

Emigration, i.e., 'brain drain'

Damascus has lost many educated people because of the civil war. There has been much less of a brain drain in Khartoum and probably none at all in Kuwait.

Muslim curriculum

Both Sudan and Kuwait have introduced a "Muslim curriculum" that focuses on teaching Islam to the relative exclusion of scientific subjects. Damascus students get only two hours of religious education per week.

Differential fertility

This factor has been studied in three Arab countries: Kuwait, Libya, and Sudan. When IQ is compared with number of siblings, there is hardly any correlation in Kuwaitis but a significant negative correlation in Libyans and Sudanese (Abdel-Khalek and Lynn 2008; Al-Shahomee et al. 2013; Khaleefa 2010). Khaleefa (2010) calculated that Sudanese IQ is declining at a rate of 0.8 points per generation because higher IQ individuals have smaller families. This factor may be stronger in Turkey, Lebanon, and Egypt, which are more Westernized.

Immigration

The Khartoum Metropolitan Area grew from 2.9 million in 1993 to 5.3 million in 2008. This growth was driven overwhelmingly by migration from South Sudan and Darfur, largely as a result of the Second Sudanese Civil War (1983-2005). As a result, “southern” migrants now make up a majority of the population:

This war led to an influx of displaced persons coming into Khartoum from the provinces and from South Sudan, now a separate state. The average IQ of Arab Sudanese with no refugee background around Khartoum has been found to be 77.4, based on UK norms. However, the average IQ of people from the war-torn region of Darfur, which is still within the current Sudanese state, is roughly 64 (Bakhiet & Lynn, 2015). This is similar to IQ estimates for the Southern Sudanese (e.g. Fahmy, 1964, cited in Lynn, 2006), many of whom also fled to Khartoum during the war (Bassil, 2013). Indeed, the genetics of the northern Sudanese is very close to that of Egypt and other North African countries. By contrast the West and south of the country are genetically closer to the Sub-Saharan Africans of South Sudan. (Dutton et al. 2017b)

Meanwhile, Kuwait became more South Asian during this same period. The IQ surveys in 2006 and 2015 thus sampled two significantly different populations:

In 1975, Jordanians and Palestinians were the predominant category comprising about 40 % of the total non-Kuwaiti population, followed by about 12 % Egyptians and 9 % Iraqis. Asians from Iran, India and Pakistan constituted only about 18 % of the non-Kuwaiti population. The Asian presence in Kuwait increased significantly during the late 1970s and early 1980s, resulting in 35 % of the non-Kuwaitis being Asian. After liberation of Kuwait, the percentage of Asians increased further and in 1995, Arabs and Asians each constituted about half of the total non-Kuwaiti population. During the decade of 1995-2005, Arabs lost ground to Asians with the latter comprising almost 59 % of the non-Kuwaiti population in 2007. (Shah 2007)


The Simber Effect

The above studies also show that IQ begins to decline during adolescence in these countries. In people of European origin the decline normally happens later in life:

The second point of interest is that in both samples the SPM score is statistically significantly lower among 18 year olds than it is among 17 year olds. In general, overall performance on IQ tests tends to increase into adulthood, meaning that we would expect 18 year olds to score higher than17 year olds. In this regard, Bakhiet et al. (2018) have identified what they have called the Simber Effect in a meta-analysis of progressive matrices administrations in 12 Arab countries. They found that IQ in Arab countries, relative to European norms, falls between the ages of 7 and 18, when looking within single cohorts. At age 7 it is the same or slightly below European norms but it eventually falls to around a standard deviation below European norms. They have shown this by comparing different cohorts divided up age, not via a longitudinal analysis of one cohort. The raw score declines at this very specific age that we have observed here would be potentially consistent with this gradual fall and they are not unique to Syria. Xhosa SPM score declines between 15 and 16 (Bakhiet & Lynn, 2015). Jordanian Advanced Progressive Matrices score peaks at 18 to 20 and then slowly declines (Lynn & Abdel-Khalek, 2009). In Sudan, SPM score peaks at 17 and then falls (Khaleefa, Lynn, Abulgasim, Dossa, & Abdulraddi, 2010) while in Somalia it also declines after the age of 17 (Bakhiet et al., In press). (Dutton et al. 2018a).

The ability to learn may have originally been a juvenile trait in our species. Childhood was a time when early humans had to learn what to do and what not to do. After puberty, they literally became set in their ways. As societies became more complex, adults had to retain this ability, in the same way they have retained the ability to digest milk sugar wherever dairy farming is practiced.


Conclusions

IQ has recently declined in parts of the Arab world, and several possible causes have been put forward. More research is needed but the following conclusions seem justified:

- Ethnic change is a major cause, if not the leading one. Although we speak of the 'migrant crisis' as a European problem, it is actually part of a larger demographic overflow from sub-Saharan Africa and South Asia, and this overflow is primarily spilling into North Africa and the Middle East. 

- Differential fertility, commonly called dysgenics, is becoming important, at least in some Arab countries. This may be due to Westernization. The upper and middle classes are more likely to follow Western models of behavior, including smaller family size. This is at most a secondary cause of declining IQ in the Arab world.

- The introduction of a 'Muslim curriculum' may or may not be a factor. Its effects on IQ should be studied in a stable Arab population that is not changing through immigration or emigration.

- The Flynn effect may be running out of steam in the Arab world, as it has in the Western world. Other trends are thus becoming visible, and those trends are largely negative. 

In itself, the end of the Flynn effect is no cause for worry. It probably does not correspond to a real increase in cognitive ability. People have simply become more adept at taking tests, including IQ tests.

Just think. Beginning at least in the 1930s the Flynn effect added around 3 points each decade to average IQ until the 1990s. Such a huge gain—18 points—should be visible in the evolution of popular culture. Yet popular culture didn't become higher-brow during that period. In fact, from the 1970s onward it became lower-brow. In magazines, fonts became bigger and sentences simpler and shorter. In movies and sitcoms, plots became less complex, and characters shallower. You could counter-argue that popular culture was now embracing the interests of ordinary people, after long being elitist, but that isn't my impression. In the 1970s I often met ordinary adults with intellectual hobbies of one sort or another, like stamp collecting, ham radio, science fiction, field naturalism, astronomy, and so on. My father had a working-class background, yet he had all the works of Ray Bradbury, plus earlier works by H.G. Wells and Jules Verne. Ordinary people like that are now hard to find, even though IQ scores have risen considerably between then and now.

This is another reason why, in the nature versus nurture debate, twin studies overestimate the latter's importance. "Nurture" is simply the residue of everything that's not nature: not only your learning environment but also your familiarity with test-taking, as well as errors in calculating test scores or differences in scores due to the way the tests are administered.  

On a final note, we need more research on IQ in the Arab world. Unfortunately, there, as here, such research is not without risk. Omar Khaleefa, at the University of Khartoum, did many pioneering studies on this subject in Sudan, including his calculation that Sudanese IQ is declining at a rate of 0.8 points per generation. He disappeared six years ago. His body was never found, and no demands for money were ever made, as is usually the case with abductions. His family holds the government responsible:

Professor Omar Haroon Al Khaleefa left his home in an upscale neighborhood of Khartoum North and was never seen again. His family holds the Sudanese authorities responsible for his disappearance, saying they have failed to investigate new information that has come to light. (Abdin 2014)


Please note:

I may or may not be posting over the next three months. This is a temporary situation, and I will resume regular posting in November.


References

Abdel-Khalek, A.M., and R. Lynn. (2008). Intelligence, family size and birth order: Some data from Kuwait. Personality and Individual Differences 44: 1032-1038.

Abdin, T. (2014).  Sudan: The Case of the Missing Professor. AllAfrica, May 22

Al-Shahomee, A.A., R. Lynn, and S.E. Abdalla. (2013). Dysgenic fertility, intelligence and family size in Libya. Intelligence 41(1): 67-69. 

Bratsberg, B., and O. Rogeberg. (2018). Flynn effect and its reversal are both environmentally caused. Proceedings of the National Academy of Sciences Jun 2018, DOI: 10.1073/pnas.1718793115 

Dutton, E., and R. Lynn. (2015). A negative Flynn Effect in France, 1999-2008-9. Intelligence 51: 67 -70. 

Dutton, E., S. Bakhiet, Y. Essa, T. Blahmar, and S. Hakami. (2017a). A negative Flynn effect in Kuwait: The same effect as Europe but with seemingly different causes. Personality and Individual Differences 114: 69 -72.

Dutton, E., S. Bakhiet, K. Ziada, Y. Essa, and T. Blahmar. (2017b). A negative Flynn Effect in Khartoum, the Sudanese capital. Intelligence 63: 51 -55.

Dutton, E., Y.A.S. Essab, S.F. Bakhietb, H.A.A. Alib, S.M. Alqafarib, A.S.H. Alfalehb, and D. Becker. (2018a). Brain drain in Syria's ancient capital: No Flynn Effect in Damascus, 2004-2013/14. Personality and Individual Differences 125: 10-13

Dutton, E., S.F.A. Bakhiet, H.A. Osman, D. Becker, Y.A.S. Essa, T.A.M. Blahmar, R. Lynn, and S.M. Hakami (2018b). A Flynn Effect in Khartoum, the Sudanese capital, 2004-2016. Intelligence 68: 82-86.

Flynn, J.R. (2009). Requiem for nutrition as the cause of IQ gains: Raven's gains in Britain 1938-2008. Economics & Human Biology 7(1): 18-27.

Flynn, J.R. (2007). What is Intelligence? Beyond the Flynn Effect. Cambridge University Press.

Khaleefa, O. (2010). Intelligence in Sudan and IQ gain between 1964 and 2008. ArabPsyNet E-Journal 25-26: 157-167.

Shah, N.M. (2007). Migration to Kuwait:  Trends, Patterns and Policies. Paper Prepared for the Migration and Refugee Movements in the Middle East and North Africa. The Forced Migration & Refugee Studies Program. The American University in Cairo, Egypt. October 23-25, 200

Teasdale, T.W., and D.R. Owen. (2005). A long-term rise and recent decline in intelligence test performance: The Flynn Effect in reverse. Personality and Individual Differences 39(4): 837-843.

Tuesday, July 31, 2018

A hardwired mental association?



Would you give this dog a male name or a female name? (Wikicommons)


Apart from any cultural or nurture-related factors, maybe we're just hard-wired to associate female with 'fair'. I have a small white fuzzy dog; everybody calls him a 'she' even though he rather obviously has a penis. However, no one assumes my small black dog is a 'she', ever."

There is an assumption that white or bright is associated with female and black or dark with the male. This sensory dimension—bright to dark—is a distinctive feature of gender and gender-related actions. There is historical and anthropological evidence that the gender categories, female-male and the sensory dimension-bright to dark-are associated. Indeed, sexual dimorphism of skin colour, namely that females have a lighter skin colour than males, is well established in research outside of the psychological literature (Semin et al. 2018).

Women are fairer-skinned than men, although the difference is smaller in very fair or very dark populations and larger in medium-colored populations (Frost 2007; Madrigal and Kelly 2007; van den Berghe and Frost 1986). This sexual dimorphism is due more or less equally to differences in melanin content and hemoglobin content of the skin. Women are thus pale in comparison to men, who look browner and ruddier (Edwards and Duntley 1939; Edwards and Duntley 1949; Edwards et al. 1941.). Parallel to this sexual dimorphism, lighter skin is mentally associated with femininity across a wide range of cultures (van den Berghe and Frost 1986).

How reflexive is this mental association? Very much so, according to a recent series of experiments with Dutch, Portuguese, and Turkish participants. In the first one, personal names were gender-identified faster when male names were presented in black and female names in white than when the combinations were reversed. In the second experiment, very briefly appearing black and white blobs had to be classified by gender; the former were classified predominantly as male and the latter as female. Finally, in an eye-tracking experiment, observation was longer and fixation more frequent when a black or dark object was associated with a male character and a white or light object with a female character (Semin et al. 2018).

We see similar results in two other studies: when given a word-association test, Navajo participants perceived the color black as more potent and masculine and the color white as more active and feminine. (Osgood 1960). In a British study, women were asked to optimize the attractiveness of facial pictures by varying the skin's darkness and ruddiness. They responded by making the male faces darker and ruddier than the female faces (Carrito et al. 2016).


Hardwired or softwired?

Is this mental association between skin tone and gender hardwired? That explanation is evoked at the outset of this paper, but toward the end the authors opt for learning:

One might well ask how this differential processing is likely to come about. One possible avenue is via the critical adaptive mechanism that humans have, namely their ability to extract regularities from their complex and noisy physical and social environments. This ability to extract regularities is automatic and is referred to as 'implicit learning' (Semin et al. 2018)

The 'implicit learning' hypothesis does not explain why this mental association is influenced by the sex hormones. Some kind of hormonal input is indicated by three studies. A brain-imaging study showed a stronger neural response in women to pictures of “masculinized” male faces, and this response correlated with their estrogen levels across the menstrual cycle (Rupp et al. 2009). In a personal communication, the lead author stated that the faces had been masculinized by making them darker and more robust in shape.

In another study, women had to choose between two facial pictures that were identical except for a slight difference in color. When male faces were shown, the darker one was more strongly preferred by women in the first two-thirds of their menstrual cycle (high estrogen/progesterone ratio) than by women in the last third (low estrogen/progesterone ratio). There was no cyclical effect if the women were judging female faces or taking oral contraceptives (Frost 1994). 

Finally, an estrogenic influence is indicated by a study of preschool children who had to choose between two dolls that differed slightly in skin color. Doll choice was the same for boys and girls. Below three years of age, however, the children who chose the darker doll had significantly more body fat than those who chose the lighter doll (Frost 1989). In that age range, estrogen is produced mostly by the body's fatty tissues (Baird 1976).

Perhaps there is both hardwiring and softwiring. People learn to associate lighter skin with women and darker skin with men. This learned mental association then interacts in the brain with a hardwired hormonal input. But why couldn't the mental association be hardwired as well? The mind tends to hardwire any recurrent task, thus shortening response time and cutting out learning time. For example, we have an innate ability to recognize faces. This is shown by prosopagnosia, a kind of brain damage where someone may seem normal and yet be no better at recognizing a face than any other object. At the other extreme are “super-recognizers” who are as good at face recognition as prosopagnosics are bad (Russell, Duchaine, and Nakayama 2009).

Then there’s that study of preschool children. Doll choice didn’t differ between the boys and the girls, but the children with more body fat had a stronger preference for darker skin, like the women during the high estrogen/low progesterone phase of their menstrual cycle. This doesn’t look like a learned preference.


References

Baird, D.T. (1976). Oestrogens in clinical practice. In J.A. Loraine and E. Trevor Bell (Eds.) Hormone assays and their clinical application, (p. 408). Edinburgh: Churchill Livingstone.

Carrito, M.L., I.M.B. dos Santos, C.E. Lefevre, R.D. Whitehead, C.F. da Silva, and D.I. Perrett. (2016). The role of sexually dimorphic skin colour and shape in attractiveness of male faces. Evolution and Human Behavior 37(2): 125-33. 

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

Edwards, E.A., and S.Q. Duntley. (1949). Cutaneous vascular changes in women in reference to the menstrual cycle and ovariectomy. American Journal of Obstetrics & Gynecology 57(3): 501-509.

Edwards, E.A., J.B. Hamilton, S.Q. Duntley, and G. Hubert. (1941). Cutaneous vascular and pigmentary changes in castrate and eunuchoid men. Endocrinology 28(1): 119-128. https://doi.org/10.1210/endo-28-1-119 

Frost, P. (1989). Human skin color: the sexual differentiation of its social perception. Mankind Quarterly 30: 3-16.

Frost, P. (1994b). Preference for darker faces in photographs at different phases of the menstrual cycle: Preliminary assessment of evidence for a hormonal relationship. Perceptual and Motor Skills 79(1): 507-14. 

Frost, P. (2007). Comment on Human skin-color sexual dimorphism: A test of the sexual selection hypothesis. American Journal of Physical Anthropology 133(1): 779-781.

Madrigal, L., and W. Kelly. (2006). Human skin-color sexual dimorphism: A test of the sexual selection hypothesis. American Journal of Physical Anthropology 132(3): 470-482.

Osgood, C.E. (1960). The cross-cultural generality of visual-verbal synesthetic tendencies. Behavioral Science 5(2): 146-169.

Rupp, H.A., T.W. James, E.D. Ketterson, D.R. Sengelaub, E. Janssen, and J.R. Heiman. (2009). Neural activation in women in response to masculinized male faces: mediation by hormones and psychosexual factors. Evolution and Human Behavior 30(1): 1-10. https://doi.org/10.1016/j.evolhumbehav.2008.08.006 

Russell, R., B. Duchaine, and K. Nakayama. (2009). Super-recognizers: People with extraordinary face recognition ability. Psychonomic Bulletin & Review 16(2): 252-257.

Semin, G.R., T. Palma, C. Acaturk, and A. Dziuba. (2018). Gender is not simply a matter of black and white, or is it? Philosophical Transactions of The Royal Society B Biological Sciences 373(1752):20170126

van den Berghe, P.L., and P. Frost. (1986). Skin color preference, sexual dimorphism and sexual selection: A case of gene-culture co-evolution? Ethnic and Racial Studies 9(1): 87-113. https://doi.org/10.1080/01419870.1986.9993516   

Tuesday, July 24, 2018

Does a fungus cause baldness?



Endgame for an ant (Wikicommons)



Is male pattern baldness (MPB) caused by a pathogen? The question may seem silly because the genetic causation is obvious. MPB is normally a male problem, and family background is important. If your male relatives go bald at an early age, the chances are good that you will too.

Genetic causation does not exclude environmental causation, however. I will argue here that a pathogen, specifically lipid-dependent yeasts of the Malassezia genus, has evolved the ability to accelerate the onset of MPB. I will also argue that this is not a side effect of infection. It is key, in fact, to the pathogen’s survival and reproduction.


The germ theory

MPB in young men was once widely blamed on a pathogen. This germ theory was first put forward by a French dermatologist, Raymond Sabouraud:

In recent years our knowledge of this subject has been much increased by the researches of Unna, Sabouraud, and others. These investigators would lead us to look upon all forms of baldness as parasitic in origin. They say that thinning of the hair, whether general or beginning on the crown or at the temples and forehead (alopecia pityrodes), can be produced by a micro- organism. [...] Sabouraud thinks the micro-bacillus of oily seborrhoea finds its way into the hair follicle and causes sebaceous hyper- secretion; then hypertrophy of the sebaceous glands; next, progressive papillary atrophy; finally, death of the hair. (Waldo 1883)

The identity of the pathogen was a matter of debate. Sabouraud attributed baldness to a bacterium and seborrhea to a yeast initially named Pityrosporum ovale and now classified as the genus Malassezia. Antimicrobials, particularly sulfur ointments and shampoos, became popular treatments for seborrhea and MPB.

This germ theory fell out of favor in the mid-20th century. Ainsworth (1956, p. 589), in his review of the literature, concluded that P. ovale was usually harmless:

During the nineteenth century it was widely held that P. ovale was responsible for the various disorders (and particularly seborrheic dermatitis) with which it is commonly associated. Sabouraud cautiously attributed pityriasis (dandruff) to P. ovale but modern opinion is even more sceptical and during the past two decades the view most generally accepted is that of Ota and Huang (1933) who after a careful experimental investigation and a study of the evidence obtained by others concluded that P. ovale is merely an inoffensive saprophyte of man.

Similarly, Ludwig (1968) wrote: "Due to a misinterpretation of the role of oil seborrhea, which so frequently accompanies the development of common baldness, Sabouraud came to the erroneous conclusion that common baldness results from a chronic infection of the scalp by his 'microbacilli'."

The medical community was in no mood to investigate Sabouraud’s germ theory any further. This was a time when causation of disease was increasingly framed in terms of genetics or lifestyle, rather than infection by a pathogen:

During the first half of the 20th century, researchers began to confront another major barrier of crypticity: long delays between the onset of infection and the onset of disease. Long delays make cause-effect linkages cryptic because other events that occur during the intervening time can form the basis of alternative causal explanations. As the delay in onset of symptoms increases, the number of such events and, hence, the number of alternative hypotheses of causation increases. The alternative hypotheses may focus on specific environmental insults, or may interpret delayed, persistent symptoms as natural wear and tear, particularly if infections are ubiquitous. (Cochran et al. 2000)

Since the turn of the millennium there has been a renewed interest in Malassezia and its role in seborrhea and MPB (Arash et al. 2002; Dawson 2007; Sastry 2004).


Going beyond the proximal cause

Today, there is a growing consensus that seborrhea is caused by the lipid-dependent yeast Malassezia, most likely the species M. globosa and M. restricta (Dawson 2007). The mode of action is less certain. Malassezia degrades sebum and releases unsaturated fatty acids, which may in turn stimulate sebum production (Dawson 2007). Alternatively, it may increase conversion of testosterone to the more active dihydrotestosterone (DHT), thus causing not only excessive sebum production but also MPB. This effect has been shown with acne, a skin condition that overlaps with seborrhea in many ways. When biopsies were taken from affected and unaffected areas in 32 subjects with acne, it was found that "acne bearing skin produced from 2 to 20 times more dihydrotestosterone than normal back skin" (Sansone and Reisner 1971).

What would Malassezia gain from DHT? We know that DHT boosts production of sebum, which contains the fat that this pathogen feeds on. Sebum may also help to shield it from the body's immune system.

There nonetheless remains one apparent flaw in this germ theory: Malassezia is common, yet only a minority of young men develop MPB. It seems, then, that some men are more genetically susceptible than others to MPB. This is part of the reason, but another reason is that some Malassezia species are better than others at altering the chemistry of the skin. The species most implicated in seborrhea are M. globosa and M. restricta (Dawson 2007). Studies of a related skin infection, Pityriasis versicolor, have found M. globosa to be more implicated than M. restricta (Saad et al 2013; Salah et al. 2005). In a review of the literature, Zarei-Mahmoudabadi et al. (2013) conclude that M. globosa is the main cause of seborrhea:

Different Malassezia species were reported as causative agents of SD in the different countries. Lee et al. (23) reported M. restricta as the most important species in Korean SD patients. In addition, Prohic (26) in a study from Bosnia and Herzegovina believes that M. restricta (27.5%) is the main agents of SD and M. globosa (17.5%) and M. slooffiae (15%) are the next agents. In a molecular study by Tajima et al. (11), M. restricta and M. globosa were detected as the predominate agents of SD. In contrast, in Hedayati et al. study in north of Iran M. globosa was reported as the most frequently agent on scalp and face lesions, whereas M. furfur had most frequency on trunk lesions (24). In the present study, out of the 110 scalp scales that were cultured on Dixons agar, 24.5% yielded Malassezia that the most frequently Malassezia species was M. globosa (40.7%), followed by M. pachydermatis (22.2%), M. furfur (11.1%) and M. restricta (7.4%).

Nine Malassezia species are found on human hosts (Dawson et al. 2018). It is likely that different species compete against each other for sites on the body surface. Colonization by an aggressively seborrheic species is thus probably impeded if another species is already present. Indeed, the relative distribution of these species varies from one ethnic group to another and from one geographical area to another (Dawson et al. 2018).


Is Malassezia sexually transmitted?

There may be another side to infection by Malassezia. It colonizes not only the scalp but also the male genital region, particularly if the man is uncircumcised:

Recently, several authors have noted Malassezia spp. as part of the microflora of healthy uncircumcised male genital regions in 49.2% of the population, in contrast to circumcised male patients, in which Malassezia spp. are identified in 22.4% of the population (2, 3). Mayser et al. assumed that Malassezia yeasts find favorable growth conditions in the lipid-rich milieu of the preputial area because of its free sebaceous glands (i.e., Tyson's glands seem to be important) (Khadar et al. 2008)

It is known that yeasts, like Malassezia, can spread from one person to another through sexual contact (Spinillo et al. 1992). The pathogen can thus enhance its own reproductive success by influencing its host's sexual behavior. Premature hair loss may therefore be one of its strategies for spreading to other hosts.

Keep in mind that men in pre-modern societies were divided into age classes, and the transition from one class to the next was determined by visible physical changes: the growth spurt of childhood, the appearance of body and facial hair in adolescence and, finally, the loss of head hair later in life. By making its host lose his head hair prematurely, the Malassezia pathogen reassigns him to a class of older men who, except for the rich and powerful, deal with sexual dissatisfaction not by divorcing and remarrying (or by finding a mistress) but rather by frequenting prostitutes. The possibilities for transmission to a new host are thus increased many times over.


Stranger things have happened

A fungal infection may actually cause sexual dissatisfaction. This kind of behavioral manipulation is not as fantastic as it may seem. Fungi are champions of such manipulation, both in overall prevalence and in sophistication:

The observation that, as a Kingdom, Fungi have many parasitic taxa [...] does not distinguish them from other major groups. Parasitism is a very common mode of life that has evolved repeatedly and probably more times than predation as a life history strategy [...]. What is notable is the apparently high frequency of parasitic fungi that have evolved not just to infect animals but also to adaptively manipulate animal behavior in ways that increase the fitness of the fungus. (Hughes et al. 2016)

You have probably heard about "zombie ants": a fungus infects an ant and reprograms its brain, causing it to leave its nest, climb up a plant, lock its jaws into the plant tissue, and die. A fruiting body then emerges from the ant's head and rains down spores on the forest floor below. There are other examples. In one case, the fungus keeps its host alive and controls its flight behavior so that the insect becomes a moving vehicle for spore release (Hughes et al. 2016).

What about humans? Greg Cochran has argued that an unknown pathogen can alter a man’s sexual orientation as a means to increase its opportunities for spreading to other hosts: "One possible route would be sexual, whereby homosexual behavior could facilitate spread because of the larger numbers of partners homosexual males may have on average, relative to heterosexual males" (Cochran et al. 2000).

Similarly, there may exist a pathogen that reverses male jealousy and makes its host desire cuckoldry, thereby gaining access to many more hosts (Frost 2013). Although many sexual fetishes are attested in the writings of ancient civilizations, cuckold envy does not seem to be one of them. The oldest references date back to 17th century England (Kuchar, 2011, pp. 18-19). The cause may thus be a sexually transmitted pathogen that entered England during the early days of the slave trade. Such a pathogen could have evolved in West Africa, where most women were in polygynous marriages, and where cuckoldry was the main route for transmission from one household to another.

We have never identified such pathogens largely because we have never bothered to look. They are also hard to find, given the delay between infection and behavioral change.


References

Ainsworth, G.C. (1958). Pathogenic yeasts. In A.H. Cook (Ed.) The Chemistry and Biology of Yeasts (pp. 587-602). New York: Academic Press.
http://krishikosh.egranth.ac.in/bitstream/1/23082/1/IVRI%20OB%201816.pdf#page=593

Arash, J., F. Sorour, and A.M. Mokhtari. (2002). Evaluation of the coincidence of Male Pattern Baldness and Pityrosporum group of fungus in Iran. Indian Journal of Dermatology 47(4): 224-226.
http://www.e-ijd.org/article.asp?issn=0019-5154;year=2002;volume=47;issue=4;spage=224;epage=226;aulast=Javanbakht;type=0

Cochran, G.M., P.W. Ewald, and K.D. Cochran. (2000). Infectious causation of disease: an evolutionary perspective. Perspectives in Biology and Medicine 43(3): 406-448.
https://doi.org/10.1353/pbm.2000.0016

Dawson, T.L. (2007).  Malassezia globosa and restricta: Breakthrough Understanding of the Etiology and Treatment of Dandruff and Seborrheic Dermatitis through Whole-Genome Analysis. Journal of Investigative Dermatology Symposium Proceedings 12(2): 15-19
https://doi.org/10.1038/sj.jidsymp.5650049 

Dawson, T.L., C. Leong, J. Goh, and A. Irudayaswamy. (2018). Geographical and ethnic differences in Malassezia species distribution on healthy skin. Congress of the International Society for Human and Animal Mycology
https://www.morressier.com/article/5ac39997d462b8028d89a224

Frost, P. (2013). First, sexual transmissibility and then ...? Evo and Proud, January 5
http://evoandproud.blogspot.com/2013/01/first-sexual-transmissibility-and-then.html

Hughes, D.P., J.P.M. Araujo, R.G. Loreto, L. Quevillon, C. de Bekker, and H.C. Evans. (2016). Chapter Eleven - From So Simple a Beginning: The Evolution of Behavioral Manipulation by Fungi. Advances in Genetics 94: 437-469.

Khadar, R.K., F. Cherif, R. Ben Hadid, M. Mokni, and A. Ben Osman. (2008). Penile shaft involvement in pityriasis versicolor. Acta Dermatovenerol Alp Pannonica Adriat. 17(2):86-9.
https://pdfs.semanticscholar.org/eaa2/e73dccf5b7cc31d8b0aa346e2d7b2db9837f.pdf

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): 1-30.

Ludwig, E. (1968). The role of sexual hormones in pattern alopecia. In A. Baccaredda-Boy, G. Moretti G, and J.R. Frey (Eds). Biopathology of Pattern Alopecia. International Symposium, Rapallo, July 1967: Proceedings. Basel, Karger, pp 50-60.
https://doi.org/10.1159/000387745

Saad, M., T. Sugita, H. Saeed, and A. Ahmed. (2013). Molecular Epidemiology of Malassezia globosa and Malassezia restricta in Sudanese Patients with Pityriasis Versicolor. Mycopathologia 175(1-2): 69-74.
https://doi.org/10.1007/s11046-012-9587-y

Ben Salah, S., F. Makni, S. Marrakchi, H. Sellami, F. Cheikhrouhou, S. Bouassida, A. Zahaf, A. Ayadi (2005). Identification of Malassezia species from Tunisian patients with pityriasis versicolor and normal subjects. Mycoses 48(4): 242-245
https://doi.org/10.1111/j.1439-0507.2005.01091.x

Sansone, G., and R.M. Reisner. (1971). Differential Rates of Conversion of Testosterone to Dihydrotestosterone in Acne and in Normal Human Skin—a Possible Pathogenic Factor in Acne. Journal of Investigative Dermatology 56(5): 366-372.
https://doi.org/10.1111/1523-1747.ep12261252

Sastry, P.S.R.K. (2004). Occult fungal infection is the underlying pathogenic cause of atherogenesis. Medical Hypotheses 63(4): 671-674.

Spinillo, A., L. Carratta, G. Pizzoli, G. Lombardi, C. Cavanna, G. Michelone, and S. Guaschino. (1992). Recurrent vaginal candidiasis. Results of a cohort study of sexual transmission and intestinal reservoir. Journal of Reproductive Medicine 37(4): 343-347.

Szasz, T.S., and A.M. Robertson. (1950). A theory of the pathogenesis of ordinary human baldness. Archives of Dermatology and Syphilology 61(1):34-48. https://doi.org/10.1001/archderm.1950.01530080040004   

Waldo, H. (1883). The causes and treatment of baldness. Bristol Med. Chir. J. 23(88): 107-113.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5043940/

Zarei-Mahmoudabadi, A., M. Zarrin, and F. Mehdinezhad (2013). Seborrheic dermatitis due to Malassezia species in Ahvaz, Iran. Iranian Journal of Microbiology 5(3): 268-271.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3895566 

Tuesday, July 17, 2018

Curly and straight



Portrait of Henriette-Marie de Buade-Frontenac, Claude Mellan (1640). Curly European hair isn’t a holdover from Africa. Europeans initially had the thick, straight, black hair of East Asians. They then evolved thinner hair with curly, wavy, and straight forms, and equally diverse colors.




Today, head hair is straight in ~45% of Europeans, wavy in ~40%, and curly in ~15% (Medland et al. 2009). As with hair and eye color, this is an unusual level of diversity for a population that is, overall, less genetically diverse than humans in general.

Straight hair is produced by different genetic pathways in Europeans and East Asians, being due to a derived EDAR allele in East Asians and to derived TCHH, WNT10A, and FRAS1 alleles in Europeans (Medland et al. 2009; Pospiech et al 2015; Tan et al. 2013). Many other alleles are likely involved (Liu et al. 2018). At first, it was thought that hair became straight in the two groups independently of each other, i.e., through convergent evolution, but ancient DNA now suggests a different scenario:

1. In a population ancestral to Europeans and to East Asians, hair became thick, straight, and long some 30,000 years ago via a derived allele at the EDAR gene (Kamberov et al. 2013).

2. This ancestral Eurasian population differentiated into a western group that would become Europeans and an eastern group that would become East Asians (Rogers 1986).

3. Thick straight hair remained prevalent in the eastern group and gradually disappeared in the western group. Nonetheless, as late as eight thousand years ago it still prevailed in half of Europeans, as shown by ancient DNA retrieved from Motala, Sweden (Mathieson et al. 2015). Today, it has an incidence of 87% in Asians and about 1% in Europeans (McVean et al. 2012; Unterländer et al. 2017).

4. In early Europeans, thick straight hair was apparently replaced by thinner hair with diverse forms ranging from curly to straight. Curly European hair is thus a derived trait, and not a holdover from ancestral Africans.

This diversification must have coincided temporally and geographically with diversification of hair and eye color, and the cause was probably the same: sexual selection of women by men in a mate market with too many unmated women. If the selection pressure is strong enough, preferences for novel visual stimuli become decisive in mate choice (Frost 2006; Frost 2014). This kind of preference was observed in a Viennese study, which found that women tend to change their hair form to less common types (Schweder 1994).

As with hair and eye color, hair form seems to have diversified in response to a stronger selection pressure than the one that caused hair to lengthen at an earlier date in ancestral Eurasians.


References

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior 27(2): 85-103.

Frost, P. (2014). The puzzle of European hair, eye, and skin color. Advances in Anthropology 4(2): 78-88. 

Kamberov, Y.G., S. Wang, J. Tan, P. Gerbault, A. Wark, L. Tan, et al. (2013). Modeling Recent Human Evolution in Mice by Expression of a Selected EDAR Variant. Cell 152(4): 691-702.

Liu, F., Y. Chen, G. Zhu, P.G. Hysi, S. Wu, K. Adhikari. (2018). Meta-analysis of genome-wide association studies identifies 8 novel loci involved in shape variation of human head hair. Human Molecular Genetics 27(3): 559-575.

Mathieson, I, I. Lazaridis, N. Rohland, S. Mallick, N. Patterson, S. Alpaslan, et al. (2015). Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528(7583): 499-503

McVean, G.A. et al. (The 1000 Genomes Project Consortium) (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.

Medland, S.E., D.R. Nyholt, J.N. Painter, B.P. McEvoy, A.F. McRae, G. Zhu, et al. (2009). Common variants in the Trichohyalin gene are associated with straight hair in Europeans. The American Journal of Human Genetics 85(5): 750-755.

Pospiech, E., J. Karlowska-Pik, M. Marcinska, S. Abidi, J. Dyrberg Andersen, M. van den Berge, et al. (2015). Evaluation of the predictive capacity of DNA variants associated with straight hair in Europeans. Forensic Science International: Genetics 19: 280-288.

Rogers, R. A. (1986). Language, human subspeciation, and ice age barriers in Northern Siberia. Canadian Journalof Anthropology 5(1): 11-22.

Schweder, B.I.M. (1994). The impact of the face on long-term human relationships. Homo 45(1): 74-93.

Tan, J., Y. Yang, K. Tang, P.C. Sabeti, L. Jin, and S. Wang. (2013). The adaptive variant EDARV370A is associated with straight hair in East Asians. Human Genetics 132(10): 1187-1191.

Unterländer, M., F. Palstra, I. Lazaridis, A. Pilipenko, Z. Hofmanová, M. Gross, et al. (2017). Ancestry and demography and descendants of Iron Age nomads of the Eurasian Steppe. Nature Communications 8(14615) 


Tuesday, July 10, 2018

It's not self-hate



Long-haired Sango woman, Democratic Republic of the Congo (Friedrich 1913, Fig. 174)



A competitive mate market will reward individuals whose secondary sexual characteristics seem abnormally bigger or flashier. A "supernormal stimulus" has a stronger visual impact than a normal one, and the behavioral response is correspondingly stronger. This effect has been studied in many animal species. When, for instance, a female butterfly passes by a male, the latter is attracted to the flashing wing pattern. The same pattern on a rotating drum exercises the same power of attraction, which increases as the speed of rotation increases—up to almost ten times the speed of a normal wing-beat (Manning 1972, pp. 47-49).  

A human example? Head hair. It has become much longer than hair elsewhere on the body, apparently because it holds some power of attraction. This lengthening has been brought about by several evolutionary changes: faster rate of growth, longer growing phase, higher density, and greater resistance to physical damage (Khumalo 2005; Loussouarn 2001; Loussouarn et al. 2005). These changes have gone farther in some populations than in others. Darwin noted "the extraordinary difference in the length of the hair in the different races; in the negro the hair forms a mere curly mat; with us it is of great length, and with the American natives it not rarely reaches to the ground" (Darwin 1936[1888], p. 906).

Long hair is the "derived" form. It evolved in those modern humans who left Africa for northern Eurasia, including some who later back-migrated to the tropics, such as the Austronesians of Southeast Asia and Oceania and the Amerindians of the tropical New World.

Short, frizzy hair is the ancestral form. Today, it is seen in sub-Saharan Africans and in some remnant groups that remained in the tropical regions of South Asia, Southeast Asia, and parts of Oceania. These groups are the Andamanese of India, the Semang of Malaysia, the Aeta of the Philippines, and the natives of Australia, Papua New Guinea, and Melanesia.


Long head hair, a component of the Kindchenschema

The ancestral hair form is straight and silky in a newborn child: "[...] the majority of African babies are not born with springy tight curls, the African child at birth is either bald or has silky loose curls similar to the Jheri curls" (Ajose 2012). This physical difference was cited by Zambian students when asked to describe how Africans look. Some of the girls "noted that African babies were born with white skin and long hair" (Powdermaker 1956).

Although adults normally have loose, silky hair in most of the world, this was not so in ancestral humans. Such hair was specific to infants and thus formed part of what Konrad Lorenz dubbed the Kindchenschema—a set of visual, auditory, and tactile cues that identifies a human infant to adults, who then feel less aggressive and more willing to provide care and nurturance (Lorenz 1971, pp. 154-164). The infant seems "cute."

This has been no less true in sub-Saharan Africa, and a desire to be similarly cute has led African women to make their own hair longer, looser, and silkier. Some of their techniques predate the colonial era:

Africa as the cradle of mankind is likely to have had hair care since the beginning of human existence. Partly because of the oral tradition of passing down history, it is difficult to corroborate evidence of hair care. But probably the earliest form of hair straightening was the molding of hair into shapes using various clays and mud (e.g., indicating the station of a married woman among the Zulu's). [...] Hair was also lengthened with fibers and grasses, much as is done for braids with synthetic extensions nowadays. Although small decorative comb-like structures have been discovered with archeological finds, it is not clear whether original Africans combed their hair or if these implements were purely decorative. Although not written down, fascinating stories of more recent hair care (and hair disasters) are often told by older women about straightening hair using hot stones even before hot combs became available. (Khumalo 2008: see also Sieber and Herreman 2000)

In 1721, John Atkins provided an early description of women braiding and dressing their hair in Sierra Leone:

[The women] work hard at Tillage, make Palm-Oil or spin Cotton, and when they are free from such work, the idle Husbands put them upon braiding, and fettishing out their woolly hair, (in which Sort of Ornament they are prodigious proud and curious) keeping them every Day, for many Hours together at it. (Sieber and Herreman 2000, p. 67)

West African women still lavish much time on their hair:

"Big hair," "plenty of hair," "much hair"—West African communities, including Mende, admire a fine head of long, thick hair on a woman. Both these elements are crucial: thickness and length. Thickness equals increase in the number of individual strands, and the length is proof of strength. Growing such luxuriant hair requires a Mende woman's patience and care. Because a man's hair is kept shaved or cut close to the scalp, people say that "men don't have hair." Beautiful hair thus is a distinctly female trait; the more of it, the more feminine the woman. (Boone 1986, p. 184)

This hairdressing tradition is ancient enough to have spawned myths, such as this one among the Mende:

It is known among Mende that all the "water people," angels, have marvelous hair. The mermaid Tingoi is known by her long, wavy hair and her glamorous habit of dressing it with a golden comb while seated on a rock. A little girl with especially long hair is feared to be in danger of drowning because she will be very attractive to the "water people," who may think she is one of them and wish her to join them. (Boone 1986, p. 192)

Long-haired women appear in the folklore of other African peoples. Among the Yoruba, a folk-tale explains "why women have long hair." A woman fell into a pit and was pulled out by her hair, which thereby became as long as a man's arm. She initially felt ashamed of her new appearance and hid herself.

But after a while she realized that her long hair was beautiful, and then she felt very proud and scorned all the short-haired women, jeering at them. When they saw this, they were consumed with jealousy, and began to be ashamed of their short hair. "We have men's hair," they said to one another. "How beautiful it would be to have long hair!"

So one by one they jumped into the pit, and their friends pulled them out by the hair.

And in this way they, and all women after them, had long hair. (Ogumefu 1929, chap V)

Another Yoruba folk-tale recounts how a king had a beautiful daughter with hair "so long that it touched the ground when she walked." But she lost her hair and regained it only after a man found a tree that bore human hair. She then became his wife. (Abrahams 1983, pp. 59-63)

Lengthening of women’s hair seems to have been most common in West Africa, but it was also practiced in central and southern Africa during early colonial times. Women of the Manyema (Tanzania) were described as having “an abundance of hair” that would “flow down to the waist in masses of ringlets” (Bettany 1892, p. 661). Among the Sango (DRC), girls old enough for marriage would plait long strands of string into their hair to create long manes (Friedrich 1913, pp. 190-191). Young women of the Mbalantu (Namibia) achieved the same effect by braiding sinew extensions (Sieber and Herreman 2000, p. 65). Nonetheless, such practices seem to have been uncommon in southern Africa. When a black South African woman traveled to the United States in the 1930s, she was struck by the number of African American women who straightened and extended their hair. “What really made me feel strange [was] nearly every girl and woman has long hair and I among them looked like a boy dressed in girl’s clothes” (Thomas 2006, p. 487).

It appears that African American women were already braiding and threading their hair at an early date. Men, however, often shaved their heads—an indication that both sexes viewed long head hair as a female ornament (White and White 1995).

In sum, hair lengthening is an African tradition that precedes colonial contact with Europeans. From the beginning, the aim was to look feminine, and not "white." The motive was not self-hatred but sexual fantasy—a desire for the supernormal, a wish to become a woman with a long mane of hair. This may be an example of humans creating in one part of the world through artificial means what has been created elsewhere through biological evolution. The same desire has been satisfied in different ways.


Evolution of long head hair in Homo sapiens

African hair can revert to the loose, silky form of infancy as a result of some illnesses: AIDS, rheumatoid arthritis, systemic lupus erythematosus, pulmonary tuberculosis with cachexia, and Behçet's disease (Ajose 2012). These illnesses somehow disrupt normal hair growth, and it is plausible that a similar disruption of genetic origin, i.e., a loss-of-function allele, was the first stage in the evolution of long head hair.

Head hair began to lengthen as ancestral humans spread out of Africa and into the temperate and arctic zones. These environments shifted the pressure of sexual selection from men to women. On the one hand, male mortality increased in relation to female mortality because men had to hunt over larger expanses of land. On the other hand, the polygyny rate decreased because it became costlier to provide for a mother and her offspring, particularly during winter. Men were scarcer on the mate market, being fewer in number and less polygynous. (Frost 2006; Frost 2014; Frost 2015).

Women were now in excess supply, and the spotlight of sexual selection was on them. Their physical characteristics became flashier, bigger, or somehow exaggerated. In the case of head hair, the existing practices of artificial lengthening helped show the way for future evolution. The cultural became biological. Over succeeding generations, the infant hair form persisted more and more into adulthood while becoming ever longer and straighter, eventually reaching down to the waist if left uncut. Hair seems to have lengthened within the whole of northern Eurasia, rather than within the smaller zone of steppe-tundra where skin became white and where hair and eyes became brightly and diversely colored. Hair lengthening was thus triggered by a lower intensity of sexual selection.

This selection pressure acted primarily on women and then secondarily spilled over onto men, perhaps because most of the genes in question are weakly sex-linked, as are most genes. Nonetheless, there is some sex linkage. Scalp hairs have a greater mean diameter and hence more volume in women, even in the shorter-haired New Guineans (Walsh and Chapman 1966). Hair growth rate and final length are also somewhat greater in women than in men (Sigler 2011, p. 13). Men furthermore tend to lose their head hair, often as early as their twenties. In general, growth of head hair is under stronger hormonal inhibition in men than in women (Kondo et al. 1990).


Conclusion

Before ancestral humans began to spread out of Africa, women were already pushing the phenotypic envelope by artificially making their hair straighter, longer, and silkier. Later, outside Africa, evolution brought this fantasy to life. As Charles Darwin concluded, such hair serves an ornamental purpose in our species: "for we know that long tresses are now and were formerly much admired, as may be observed in the works of almost every poet; St. Paul says, "if a woman have long hair, it is a glory to her." (Darwin 1936[1888], p. 906).


References

Abrahams, R.D. (1983). African Folktales. Traditional Stories of the Black World. New York: Pantheon Books.
https://books.google.ca/books?id=JqJVU4XYvLYC&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

Ajose, F.O.A. (2012). Diseases that turn African hair silky. International Journal of Dermatology 51 (supp. S1): 12-16.
https://doi.org/10.1111/j.1365-4632.2012.05556.x

Bettany, G.T. (1892). The World’s Inhabitants or Mankind, Animals, and Plants. London: Ward, Lock, Bowden and Co. 
https://books.google.ca/books?id=mkBOAQAAMAAJ&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

Boone, S.A. (1986). Radiance from the Waters: Ideals of Feminine Beauty in Mende Art. New Haven and London.
https://books.google.ca/books?id=anjOC0zZ6kgC&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

Darwin, C. (1936 [1888]). The Descent of Man and Selection in relation to Sex. reprint of 2nd ed., The Modern Library, New York: Random House.

Friedrich, A. (1913). From the Congo to the Niger and the Nile. An account of the German Central African Expedition of 1910-1911 by Adolf Friedrich Duke of Mecklenburg, vol. 1. London: Duckworth and Co.
https://archive.org/stream/fromcongotonige01adol/fromcongotonige01adol#page/n5/mode/1up

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior 27(2): 85-103.

Frost, P. (2014). The puzzle of European hair, eye, and skin color. Advances in Anthropology 4(2): 78-88. 

Frost, P. (2015). Evolution of long head hair in humans. Advances in Anthropology 5(4): 78-88.

Khumalo, N.P. (2005). African hair morphology: macrostructure to ultrastructure. International Journal of Dermatology 44(Suppl. 1): 10-12.

Khumalo, N.P. (2008). On the history of African hair care: more treasures await discovery. Letter to the Editor. Journal of Cosmetic Dermatology 7(3): 231.

Kondo, S., Y. Hozumi, and K. Aso. (1990). Organ culture of human scalp hair follicles: effect of testosterone and oestrogen on hair growth. Archives of Dermatological Research 282(7): 442-445.

Lorenz, K. (1971). Studies in Animal and Human Behaviour, vol. 2. London: Methuen & Co.

Loussouarn, G. (2001). African hair growth parameters. British Journal of Dermatology 145(2): 294-297.

Loussouarn, G., C.E. Rawadi, and Genain, G. (2005). Diversity of hair growth profiles. International Journal of Dermatology 44(Suppl. 1): 6-9.

Manning, A. (1972). An Introduction to Animal Behaviour. 2nd edition. London: Edward Arnold.

Ogumefu, M.I. (1929). Yoruba Legends. London: The Sheldon Press. 

Powdermaker, H. (1956). Social change through imagery and values of teen-age Africans in Northern Rhodesia. American Anthropologist 58(5): 783-813.
https://doi.org/10.1525/aa.1956.58.5.02a00030 

Sieber, R. and F. Herreman. (2000). Hair in African Art and Culture. African Arts 33(3): 54-96.
http://homework.sdmesa.edu/drogers/Art%20115/sieber%20hair%20in%20african%20art.pdf

Thomas, L.M. (2006). The modern girl and racial respectability in 1930s South Africa. Journal of African History 47(3): 461-490
https://doi.org/10.1017/S0021853706002131

Walsh, R.J., and R.E. Chapman. (1966). A study of the quantitative measurement of human head hair fibres. Man, new series. 1(2): 226-232.

White, S. and G. White. (1995). Slave Hair and African American Culture in the Eighteenth and Nineteenth Centuries. The Journal of Southern History 61(1): 45-76.