Sexually dimorphic traits are associated with subsistence strategy in African faces from the Sahel/Savannah belt

doi:10.21203/rs.3.rs-2802336/v1

Download PDF

Article

Sexually dimorphic traits are associated with subsistence strategy in African faces from the Sahel/Savannah belt

https://doi.org/10.21203/rs.3.rs-2802336/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 28 Oct, 2023

Read the published version in American Journal of Human Biology →

Version 1

posted

You are reading this latest preprint version

Previous research revealed that in some African populations, food-production strategies are associated with facial shape. Nomadic pastoralists living in the African Sahel/Savannah belt have a different facial morphology than their sedentary neighbours. We investigated whether the lifestyle associated with a subsistence pattern has an impact on sexual dimorphism in the facial structure. We employed several methods from geometric morphometrics and demonstrated such effect in four ethnically distinct populations that share the same geographic space. We show that the facial traits which correlate with a subsistence strategy are systematically associated with levels of facial sex-typicality. In particular, we found that faces with more pronounced pastoralist features have on average more masculine facial traits and that this effect is more pronounced in men than in women. In general, though, the magnitude of overall facial dimorphism does not differ between pastoralists and farmers. Pastoralists (in contrast to farmers) tend to have a more masculine facial morphology but facial differences between the sexes are in both groups the same.

Health sciences/Anatomy

Earth and environmental sciences/Ecology/Behavioural ecology

Biological sciences/Evolution/Anthropology

Biological sciences/Evolution/Anthropology/Biological anthropology

Sexual dimorphism

Subsistence

Geometric morphometrics

Human face

Africa

Sexual dimorphism has a massive impact on the overall architecture of the human body, affecting many dimensions of human life. Differences between the sexes are apparent in faces but variation in facial sexual dimorphism across human populations is substantial and its evolutionary role is not yet sufficiently well understood ^1–5. Previous studies focused on comparisons between hunter-gatherers and food-producers (mostly traditional farmers vs. industrial populations) and investigated mainly the health status related to physical activities and the diet ⁶.

Some studies suggested that in hunter-gatherers, we find a higher level of sexual dimorphism than in food-producers due to more pronounced differences between physical activities and mobility in men and women ⁷. This scenario seems to reflect a simplistic assumption about gender roles which can, however, vary substantially among the different hunter-gatherer groups, including those that inhabit sub-Saharan Africa ^8–10. Later models considered the role of specific task allocation and overall level of physical activity while paying more attention to the range of behavioural responses to environmental conditions that result from various energetic and reproductive trade-offs ¹¹. Unfortunately, morphological differences between the sexes and sexual dimorphism in different food-producing groups – such as pastoralists and farmers – tended to be neglected.

The form and extent of sexual dimorphism of various parts of human body (except for the pelvis with its strong dimorphism; ¹²) is population-specific, which has some important forensic implications ¹³. Sexual dimorphism is a highly important component of biological variation of our body, but it is also important to understand which factors affect its expression. It seems that sexual dimorphism has been associated with subsistence strategy in both past and recent human populations ¹⁴.

There is an apparent link between the anatomy of cranial architecture, development of masticatory muscles affecting the bite force, and the subsistence mode in both human and non-human animals^15,16. This link has a polygenic foundation ^17,18 but some genes can have a wide impact. If we compare modern humans and great apes, reduction of the masticatory apparatus may have been due to just one specific deletion in the MYH16 gene which took place in our ancient ancestors. In fact, this simple mutation event may have had a pleiotropic effect: in addition to reducing the masticatory apparatus, it also affected encephalisation in the lineage leading to humans ^19,20. On the other hand, it seems that the development of neurocranial and brain structures were two independent processes ²¹.

With respect to facial sexual dimorphism, previous research described sex differences in the masticatory apparatus, which may have played an important role in the evolution of not only facial but overall cranial morphology ^1,22. This research had also highlighted population affinity in sexual dimorphism of the face, while explaining these shared patterns by sex differences in masticatory functions ¹. It suggests that in various human populations, sexual dimorphism may have evolved hand in hand with the evolution of masticatory apparatus whose development would have reflected the prevailing subsistence strategy.

Our study examines the facial morphology of Africans from four populations with known ethnic affiliation and subsistence strategy. Members of our target populations inhabit the same environmental region (the Sahel/Savannah belt of Africa) but differ in their subsistence strategy: they depend either on pastoralism or on agriculture, which are two alternative survival strategies in the studied region. Moreover, because the scheduling of economic activities of these peoples in the course of the year differs, it is difficult for any group to combine pastoralism with farming ²³.

There are two main ethnic groups of pastoralists in the Sahel/Savannah belt of Africa: the Fulani in the west and the Arabs in the east, whereby the two are in contact in the area of Lake Chad Basin²⁴. The Fulani stand out not only by strong ties to their huge cattle herds but also by their non-typical sub-Saharan physical features, which are likely due to the fact that their ancestors had in distant past mixed in northern Africa with a Eurasian population ^25,26. In the eastern part of the Sahel/Savannah belt live the Arabs. They are the descendants of several Bedouin tribes which originated in Arabia, in the seventh century CE began to infiltrate northern Africa, and later moved further south and beyond the Sahara ^27,28. Originally, they bred camels but some of their groups, such as the Baggara (word means in Arabic ‘cow’), began to specialise in cattle breeding after a contact with the Fulani in the 17th century. It means that both groups of these Sahelian pastoralists nowadays evince genetic signatures of admixture. While the Arabs had originally Eurasian ancestry and secondarily acquired an admixture due to a gene flow from sub-Saharan Africa, the opposite holds of the Fulani ^25,29,30.

In addition to the pastoralists, the Sahel/Savannah region is inhabited by a high number of relatively small ethnic groups of farmers. Possibly due to isolation by distance (IBD) seen in their gene pools ³¹, languages of these sedentary peoples diversified more rapidly than the languages of mobile pastoralists who maintained closer contacts throughout the Sahelian space thanks to their migration patterns and matrimonial networks. Nowadays, we can distinguish three main groups of sedentary farmers in the Sahel/Savannah belt: Chadic-speaking peoples (branch of the Afro-Asiatic family), Nilo-Saharan speakers, and Niger-Congo speakers. Interestingly, these peoples bear much less of the Eurasian genetic component (if any) than their pastoralist neighbours. This can be clearly demonstrated by analyses of their uniparental genetic markers ^32–34 or nuclear SNP variants ^25,26.

The present study aims to explore associations between the lifestyle (subsistence strategy) and facial patterns of sexual dimorphism in certain rarely studied populations in the Sahel/Savannah belt. We want to explore the level of sex differences in the face and investigate whether the prevailing mode of food production is associated with the degree of sexual dimorphism in the human face. We expect that the nomadic lifestyle (pastoralism), associated with long-range mobility (transhumance) and demanding conditions that require more sexual division of labour, would be associated with higher levels of sexual dimorphism irrespective of the genetic/ancestry composition of the population studied, while the sedentary lifestyle (pastoralism), where physical activity is less divided by sex, would be associated with a reduction of sexual dimorphism.

In fact, the main concern for Sahelian pastoralists is making sure that the daily consumption of energy required to move from camp to camp or from a camp to pasture and/or watering points does not exceed the energetic yield the herd receives. They must therefore choose the place to break camp judiciously and respond to the requirements of their large herd regardless of the effort it requires of them. Naturally, these calculations regarding energy gained must include the time and energy spent drawing water (mostly manually), which is often located in deep wells so that considerable energy is expended on acquiring sufficient quantity for their thirsty animals ³⁵. It should be noted that it is rather difficult to measure, precisely and reliably, the energy expenditure, food intake, and disease burden in the Sahelian pastoralists and farmers, because all these variables strongly depend on the season and long-term data are very difficult to obtain in the field ³⁶.

In connection with this way of life, which is full of hardship especially during the dry seasons, it has been shown that the fertility of pastoralists is lower than that of farmers. In almost all groups of Sahelian pastoralists, one can observe several phenomena which reduce population growth. Among the pastoralists, one finds higher sterility rates in women, higher sex ratios for men, longer breastfeeding, later marriages, and higher marital instability ³⁷. These phenomena are not just ethnically linked: they are observed even where groups belonging to the same ethnicity differ only in their subsistence strategy, that is, when comparing pastoralists with farmers belonging to the same ethnic group.

In general, there are several reasons to assume that nomadic pastoralists do have generally harder and more demanding way of life because they had to invent various strategies to survive in a climate as harsh and climatically unstable as the Sahel is ³⁸. On the other hand, some studies on East African pastoralists suggest that they may have a better diet, especially when measuring protein intake in children (35 g/day in settled Turkana vs. 73 g/day in nomadic Turkana), which is largely due to milk consumption ³⁹. This particular difference between pastoralists and farmers in the Sahel/Savannah space is supported by clear genetic evidence, which shows that pastoralists are capable of consuming large quantities of fresh milk even in adulthood ⁴⁰.

It has been shown that in the Sahel/Savanna region, the mode of subsistence is associated with a particular facial shape ⁴¹. In the present study, we further test whether the facial features associated with the mode of subsistence are systematically linked with facial traits reflecting sex-typicality. We do not necessarily expect that a particular degree of sexually dimorphic traits in either subsistence group evolved as a result of direct selection on sex-typical facial traits due to the subsistence strategy. Rather, we suggest that shape changes in faces are secondarily caused by overall changes in body structure which take place in response to a particular lifestyle linked with a subsistence strategy. Specifically, we hypothesise that the more demanding pastoralist lifestyle, which goes hand in hand with higher energy expenditure but most likely also a better diet based on milk consumption in all age cohorts (with the requisite genetic adaptation), elicits a positive pressure on an increase in body musculature (higher protein intake) and a reduction of fat deposits (higher energy expenditure related to higher mobility). In other words, we expect pastoralism to be associated with changes in body constitution which are usually linked to masculinisation. In this respect, it should be noted that the higher stature of East African pastoralists has been attributed to the benefits of milk consumption ⁴². We therefore expect that facial traits which reflect the differences along the pastoralist – famer axis should be systematically associated with sex-specific variation, so that nomadic pastoralism would favour the more masculine range of facial shape variation, while sedentary farming rather the feminine side.

The subjects and acquisition of facial photographs

The Sahel/Savannah belt is a semi-desert environment lying between the Sahara and tropical rain forests, where pastoralism is quite prominent. In the Sahel states, pastoralists are sometimes marginalised, but they do contribute a significant share of GDP in the agricultural sector ⁴³. Pastoralists and farmers engage in various types of interactions. While farmers tend to supply the market with grain and vegetables, pastoralists contribute meat and dairy products. The two thus need each other for mutual exchange of products. On the other hand, they also at times engage in disputes over access to water and land, which can lead to serious conflicts. The behavioural (lifestyle) differences between these two groups are clear, especially regarding their mobility: while farmers are settled around their fields, build grain supplies in granaries, and live in permanent villages for generations, pastoralists engage in transhumance and roam the countryside with their herds ⁴⁴.

In our study, pastoralist groups included the Fulani and the Arabs. Fulani portraits were collected in Chad (in the vicinity of Bongor and Linia), Cameroon (in Tcheboua), Niger (in Diffa, Abalak, Ader, Balanungur, and Zinder), Burkina Faso (in Banfora and Tindangou), and Mali (in Diafarabe). Arab images were collected in Chad (in Mao) and in Nigeria (in Ngala). Photographs of farmers belong to the Afro-Asiatic Chadic-speaking peoples were collected in Cameroon (the Bulahay in Mokolo, the Hide in Tourou, the Kotoko in Holouf, the Mafa in Soulede, and the Masa in Yagoua) and in Niger (Buduma in Balatungur). Images of the Nilo-Saharan speaking farmers were collected in Chad (the Kanembou in Mao), Nigeria (the Kanuri in Wodai, Dikwa, and Ngala), and Mali (the Songhai in Hombori). See Fig. 1 for geographical distribution of the studied populations.

All photographed persons were instructed to gaze directly at the camera while keeping a neutral facial expression and to avoid any head tilting or other deviations from the Frankfort horizontal plane. All possible efforts were taken to ensure uniform settings, especially with respect to preventing any photographic distortions among the different individuals or datasets. Images were taken by Nikon D70 with a fixed focal length of 50mm. Distance between the camera and the subject was set at 125cm. All pictures were taken during the dry season, which in the Sahel corresponds approximately to a period between December and March. In total, the study includes 289 photographs of men (Age Mean ± SD: 40.36 ± 15.18, range: 13–80) and 151 women (Age Mean ± SD: 32.15 ± 11.14, range: 13–63). For further information about sample distribution, see Table 1.

All procedures used in the study were approved by the Institutional Review Board of the Faculty of Science of the Charles University (protocol ref. no. 04/2020). All individuals involved in this study provided informed consent and agreed with inclusion of the physical data, which they provided for scientific purposes. All the experiment protocol for involving humans was in accordance to guidelines of national/international/institutional or Declaration of Helsinki.

Table 1

Sample distribution across target populations
Population	Men
	N	Mean Age	SD	Range	N	Mean Age	SD	Range
ARA	44	41.2	15.4	20–80	18	35.6	9.8	20–50
FUL	107	43.2	16.1	14–70	77	31.0	12.5	13–60
CAD	104	42.9	15.5	13–80	34	34.4	12.8	18–63
NLS	34	34.2	13.7	14–60	22	27.6	9.4	16–47
ARA – Arab pastoralists, FUL – Fulani pastoralists, CAD – Chadic farmers, NLS – Nilo-Saharan farmers

Geometric morphometrics

To capture facial shape variation, we defined on each face 47 landmarks, 15 of which were denoted as semilandmarks that describe curves and outlines. For definitions and locations of landmarks and semilandmarks, see our previous work ⁴¹. Facial shape coordinates represented by landmarks and semilandmarks were superimposed by Generalised Procrustes Analysis using the gpagen () function in the Geomorph package in R ⁴⁵. Semilandmarks were slid along the tangent direction and their positions optimised by algorithm that minimises the bending energy between corresponding points. Subsequently, the facial configurations were symmetrised along the bilateral axis ⁴⁶. This was done in the following steps: The x-coordinates of all landmarks were first multiplied by -1, then the bilaterally paired landmarks were relabelled, meaning that paired landmarks on the left side were given the labels of landmarks on the right side and vice versa. Finally, the original and mirrored landmark configurations were averaged.

Scores of sex-typicality, i.e., the morphological level of individual development of sexually dimorphic traits, were computed using aligned symmetrised shape coordinates that resulted from the joint Procrustes fit of female and male facial symmetrised configurations. First, we determined the vector in facial morphospace which connects the sex-specific averages. This vector of sex-typicality defines shape differences between the men and the women. Second, individual sex-typicality scores were computed by projecting each face onto the vector between sex-specific means. Scores related to female configurations were inverted (multiplied by − 1) so that higher values would be interpreted as higher levels of sex-typicality for both men (higher masculinity) and women (higher femininity).

The shape scores of subsistence mode, which reflect shape variation along an axis defined by pastoralist and farmer means, were calculated separately for male and female faces based on a Procrustes residual that resulted from the joined Procrustes fit of symmetrised shape coordinates of both subsistence groups. Each face was then projected onto the vector connecting mean pastoralist and mean farmer configuration. Scores corresponding to pastoralist faces were inverted to ensure that higher values indicate higher levels of subsistence mode typicality.

Shape changes associated with the vector of sex-typicality and subsistence mode were visualised by thin plate spline interpolation function using plotRefToTarget () function in the geomorph package ^45,47,48. All statistical analyses, scatterplots, thin-plate spline extrapolations, and combined graphs were performed in R 4.0.4.

Measurement error was assessed in terms of repeatability on a subsample of 24 faces. Each face was digitised twice by the same digitiser. Using procD.lm () function, we ran a Procrustes analysis of variance between individual faces and two digitised configurations (replicates) of the same face. Repeatability was quantified as the ratio of two variances components. The component of interindividual variance was divided by the sum of interindividual and measurement error variance components. Repeatability of digitising precision between the two replicates was 0.983, which indicates measurement error below 2%.

Statistical analysis

To examine the impact of sex and subsistence on facial morphology, we built a model with facial shape as a dependent variable and the main effects of sex and subsistence mode and their interaction as predictors. This was done using procD.lm () function from the geomorph package. General linear models (lm () function in base R) were used to test whether there are any differences in the degree of sexual dimorphism between the subsistence mode groups and to examine possible associations between the scores of facial shape dimorphism, subsistence mode, and sex. A trajectory analysis was employed to compare the direction and length of sex-related vectors in the facial morphospace between men and women of populations belonging to the two subsistence groups ^49,50.

First, we inspected variation in the distribution and range of facial shape dimorphism (SShD) in four target populations. This comparison showed only subtle differences in the overall magnitude and distribution of SShD as demonstrated by violin plots on Fig. 2 (see also Supplementary figure S1 for age-residualised SShD and Supplementary figure S2 for a comparison of present results with the situation in eight other populations published in ⁵).

Procrustes ANOVA revealed that sex, subsistence mode, and their interaction have a significant effect on facial shape. The results are summarised in Table 2. When the varying effect of population was added to the model, meaning that we accounted for the potentially confounding effect of differences between populations above categorisation by the mode of subsistence, the result did not change (see Supplementary table S1). A statistically significant interaction effect between sex and subsistence mode indicates that shape variation associated with the mode of subsistence does not equally affect the facial morphology of both sexes.

Table 2

Summary statistics for a model that quantifies the relative amount of shape variation attributable to sex, mode of subsistence, and their interaction.
	Df	SS	MS	F	Z	p-value
Subsistence	1	0.029	0.029	5.161	3.758	0.001
Sex	1	0.04	0.04	6.942	4.211	0.001
Sex:Subsistence	1	0.017	0.017	2.981	2.523	0.006
Residuals	436	2.4867	0.006
Total	439	2.644

Notes: Df – degrees of freedom, SS – sum of squares, MS – mean squares

To disentangle how facial variation due to the mode of subsistence affects the facial features responsible for sexually dimorphic variation, we built a model where SShD scores (response variable) are predicted by subsistence mode shape scores, sex, and their interaction. Faces with more pronounced pastoralist features have on average also more masculine facial traits. (See Fig. 3 for visualisation of the relationship between morphological sex-typicality and shape traits associated with the subsistence mode.) Interaction between sex and the mode of subsistence indicates that this effect is significantly more pronounced in the faces of men than in the faces of women (β = 0.0235, t = 1.977, p = 0.0487); see also Supplementary table S2 for a summary of results. Shape variation due to sexual shape dimorphism in the faces of pastoralists and farmers is visualised by TPS deformation grids in Supplementary figure S3.

When the model was extended by the potentially confounding variables of individual’s age and body height, the relationship between SShD and subsistence mode remained statistically significant (β = 0.362, t = 2.634, p = 0.009). Neither age (β < 0.001, t = 0.794, p = 0.428) nor body height (β < 0.001, t = 1.841, p = 0.067) have a significant effect on SShD. Note that this calculation was done based on a reduced dataset of 239 individuals for which we had information regarding their body height.

Pastoralists and farmers display comparable levels of facial dimorphism. An analysis of variance with factors of sex, subsistence mode, and interactions between them revealed that pastoralists and farmers do not statistically differ in their average level of sexual dimorphism (see Supplementary table S3).

Trajectory analysis yielded a similar image (see Fig. 4 and Supplementary tables S4 and S5). We found no statistically significant differences in the magnitude of sexual dimorphism between the examined populations. Variation in the direction of sexual dimorphism was notable but small, with a statistically significant angle between the Nilo-Saharan farmers and Arab pastoralists (θ = 66.8°, p = 0.013) and between the Chadic farmers and Fulani pastoralists (θ = 46.31°, p = 0.046).

In this study, we provide evidence in support of the hypothesis that food-production strategy is systematically associated with facial sex-typicality. Pastoralists living in the Sahel/Savannah belt have a more masculine facial morphology than farmers in the same region do, and this effect is more pronounced in the faces of men than in the faces of women. Our results thus corroborate a previous finding that pastoralists and farmers differ in their facial morphology ⁴¹ and newly add that the subsistence mode is significantly associated with facial shape variation due to sex differences. The overall nature of shape changes associated with sexual dimorphism is similar in both subsistence groups. Women have a more gracile facial structure with a reduced lower face and smaller nose, while men have a wider chin and a broader and larger nose. Pastoralist men – and to a lesser degree also pastoralist women – have larger lower faces than the farmers do (see Supplementary figure S3). This morphological pattern backs up our main finding about the higher level of masculinisation in the facial structure of nomadic peoples in the Sahel/Savannah belt of Africa.

Classic research into human height dimorphism hypothesised that agricultural societies should exhibit a lower degree of sexual dimorphism in stature than non-agricultural societies due to sex differences in labour division ^51,52. It soon turned out, though, that support for the notion that equal division of labour correlates with lower levels of sexual dimorphism is unclear ⁵³. Our study questioned the analogous effect for facial morphology. Along a similar vein, our results indicate that a more equal division of labour in sedentary farmers is not associated with a decrease in the magnitude of facial sexual dimorphism.

In literature, we find references to several factors which have been claimed to influence the sexual dimorphism of human face. Many studies attempted to explain facial dimorphism as a consequence of human mating behaviour. In contrast to other parts of human body, face is only rarely hidden, thus enabling an immediate detection of an individual’s sex even in climatic and/or social conditions which necessitate the covering of other sex-typical body traits. While female facial femininity is universally preferred across cultures, the relation of male facial masculinity to mate choice is far less straightforward ^54–57. While men tend to prefer feminine women across cultures, there are some differences between populations in the magnitude of this preference ⁵⁸. Neither cross-cultural differences in facial shape variation, sex differences in body height, nor differing preferences for facial femininity and masculinity across countries explain the observed patterns of facial dimorphism. A quantitative comparison based on eight distant human populations showed that the association between sexual shape dimorphism and attractiveness is moderate for women and weak or none for men ⁵⁴. Moreover, female preference of male facial masculinity seems to be mediated by a wide array of biological, psychological, and ecological variables including the menstrual phase of the observer, type of relationship, self-esteem, use of hormonal contraception, environmental conditions, and various combinations of the above ^59–64

A subsidiary factor that may affect the male part of human facial dimorphism is women’s preference for taller and stronger men. Facial morphology is affected by overall body size ^65–67. In particular, taller and heavier men are not only perceived as more masculine ⁶⁸, but taller men also have a more masculinized facial structure ⁶⁹. Height is also associated with male health: tall (but not the tallest) men seem to have optimised immunity function ⁷⁰. In general, male tallness is preferred across human societies, but no such simple preference exists or female height ^71–73. Greater body mass, on the other hand, might be costlier in regions with uncertain food availability. Greater mass may also be disadvantageous for hunting, as indicated by the negative correlation between body size and food returns in African hunter-gatherers ⁹. For instance, Tanzanian Hadza women do not prefer taller men⁷⁴. In fact, they are more likely to marry men shorter than themselves ⁷⁵. Likewise, the Himba nomads from northern Namibia show preference for equal height in both sexes ⁷⁶. Still, a recent cross-population comparison showed that sex differences in body height predict the average sex differences in facial morphology but do not explain the overall variation of SShD, such as range and distribution, across populations as such ⁵.

Yet another possibility is that sexual dimorphism is driven by intrasexual competition between males, so that stronger and more masculine males are able to provide various direct and indirect benefits, which ultimately allow them to reproduce more effectively. A recent metanalysis revealed that male body muscularity is the strongest and sole consistent predictor of mating and reproduction ⁷⁷, while facial robustness/masculinity predicts neither of these outcomes. It is thus possible that facial masculinity is not the result of direct selection but rather a by-product of the evolutionary forces that act primarily on testosterone-dependent traits of the male body. Evolutionary causation is usually recursive, meaning that once a particular sex-typical trait in human faces appears, it can be co-opted for various biosocial functions which, in turn, may shape this particular facial trait even further. Altogether, currently available evidence does not allow us to determine what is the dominant force shaping human facial dimorphism.

Therefore, we do not interpret the observed relationship between facial sex-typicality and subsistence as necessarily functional, although it would be premature to a priori reject this possibility in light of evidence regarding the association between cranial anatomy, the development of masticatory muscles, and subsistence in both human and non-human animals ^1,15,16,22. Rather we hypothesise that the more demanding pastoralist lifestyle that goes hand in hand with higher energy expenditure related to higher mobility, but most likely also a better and protein rich diet (based on milk and meat consumption), imposes a developmental pressure on the growth of body musculature and reduction of fat deposits. In short, pastoralist lifestyle is associated with changes in body constitution towards masculinisation. Taking together all the above-mentioned evidence, ^5,56,77 we suggest that a more likely scenario is that human facial dimorphism is not the result of a direct selection that acted on craniofacial morphology. Rather, the shape changes in craniofacial constitution are a secondary by-product of overall autocorrelated changes in bodily constitution and musculature. As a result, the harder and physically more demanding lifestyle of nomadic pastoralists shifts the morphological traits in facial morphospace more towards the masculine range. This contrasts with the less active sedentary farmers whose faces are shifted towards the less masculine (more feminine) range. Our research in the Sahel/Savannah belt of Africa had shown that most pastoralists are capable of digesting milk sugar in adulthood because they have a genetic variant that causes lactase persistence ⁴⁰. As a result, they can and do safely consume fresh milk with great calcium content in great quantity. Moreover, it can be shown that in pastoralists, this trait is under a strong positive selection pressure ^25,78,79. In Sahelian farmers, on the other hand, the incidence of lactase persistence is close to zero ⁴⁰. Such surprising association of this specific trait with the mode of subsistence in sub-Saharan Africa is in clear contrast with its distribution in Europe, where lactase persistence closely correlates with longitude and is thus geographically based (northern Europeans have a higher frequency of this trait than people in central and especially southern Europe). We can thus deduce that thanks to increased calcium intake, the bones of both northern Europeans and Sahelian pastoralists might achieve a more robust, and therefore more masculine, appearance especially when hardship supports such development throughout their lives.

In this context, one could also mention the differences in metabolic pathways between the pastoralists and farmers in the Sahel. This variation can be viewed as a specific response to the natural environment in which a population spends most of the time ⁸⁰. In the Sahel/Savannah belt, we found differences between the pastoralists and farmers when studying the NAT2 gene (Arylamine-N-acetyltransferase 2), which is involved mainly in the metabolism of xenobiotics but might also have some function in the immune system ⁸¹. It has been shown that pastoralists belong more frequently to the slow (as opposed to fast) acetylator phenotypes ⁸², meaning that detoxification in their organisms is generally slower than in farmers, which might be a risk factor especially when they seasonally move to different xenobiotic environments. For individuals with the slow acetylation phenotype, such environments might be especially challenging.

Interesting differences between the pastoralists and farmers of the Sahel/Savannah belt were revealed by an investigation of correlations between genetic distances, geography, and language ³¹. In farmers, genetic distances between pairs of farming populations correlate with their geographic distances but not with their linguistic distances. This phenomenon is even more pronounced in the maternally inherited genetic systems, such as mitochondrial DNA, than in paternal loci, such as the non-recombinant part of Y chromosome. Pastoralist population pairs, on the other hand, show more of a correlation between genetic and linguistic distances, and this applies to both maternal and paternal genetic loci. This implies that isolation by distance might have had a greater impact on farmers (and especially on female farmers) than on pastoralists. In short, it demonstrates the effects of sedentism and patrilocality in farming populations. Moreover, a study of gene flow between pastoralists and farmers suggested that pastoralists have a lower effective population size because they lose their females by an asymmetric matrimonial pattern ⁸³. Interestingly, this pattern has been found also in other African populations that maintain a different lifestyle ⁸⁴.

One unexpected outcome of our study is the finding that the magnitude of sexual dimorphism in sub-Saharan Africa varies substantially. Newly obtained data from the Sahel/Savannah belt suggest that both pastoralists and farmers show relatively high levels of sexual dimorphism. These levels are much higher than in populations of Bantu origin and comparable to facial sex-differences in people of European and South American origin (see Supplementary figure S2). Recent study revealed a low level of facial sexual dimorphism in the Maasai, which is surprising given the high level of sexual body dimorphism in this population ². This joint evidence indicates that facial dimorphism in sub-Saharan Africa might be lower than in the Sahelian belt. The only exception are the Chadic farmers, who evince a lower range of sexual dimorphism on a level similar to the Namibians.

One could well ask whether the population-specific differences in sexual dimorphism could be explained by a coevolution of subsistence and mating strategies. In contrast to mobile foragers, sedentary agricultural societies, which enjoy the benefits of food production and storage technologies, are prone to accumulation of resources and thus also their unequal distribution⁸⁵. A comparison of data from hunter–gatherers, herder–horticulturalists, and intensive farmers/fishermen support the view that cultural innovations, such as herding and farming, can increase the variance in reproductive success, and that this can affect even predominantly monogamous societies⁸⁵. If there was in farmers a greater variance in lifetime reproductive success (e.g., due to the degree of monopolisation of women) than in pastoralists, one would then expect that farmers evince greater levels of sexual dimorphism. Our results, however, show that the magnitude of facial SShD is approximately similar in both subsistence groups. Moreover, much lower sexual dimorphism compared to Sahelian populations was found in the Cameroonians of Bantu origin who live in both urban and rural areas ⁵. This indicates that environmental factors and way of life need not affect the range of sexual dimorphism and that phylogenetic relationships need to be taken into account in future multi-population comparisons of the magnitude and patterns of facial dimorphism. Although our present data show that patterns of sexual dimorphism vary substantially within Africa, more research is needed to complete the overall image of dimorphism variations on this highly diverse continent.

It is yet to be seen whether the observed difference in facial masculinisation between farmers and pastoralist is due to a feminisation of farmers’ facial features or due to a masculinisation of pastoralist faces. To answer this question, we would need to know more about the plesiomorphic morphological setup of male and female facial morphology in members of an ancestral population from which the recent populations of the African Sahel/Savanah belt emerged. A promising approach would be to map the facial shape of target populations on their phylogenetic tree in order to assess their ancestral morphology. Estimated ancestral morphology of male and female faces, including the characteristics of ancestral sexual dimorphism, would be subsequently compared with recent pastoralists and farmers. But a robust analysis of this kind would require a large dataset of facial morphologies associated with information about genetic background on an individual level.

Based on four rarely studied populations from the African region of Sahel/Savannah, we examined the hypothesis that subsistence strategy is systematically associated with the level of sexual dimorphism in human face. The main finding of our study is that the faces of nomadic pastoralists have on average more masculine facial features than the faces of sedentary farmers who live in the same geographic space and climate. We speculate that the reported association between facial sex-typicality and subsistence is likely due to differences in food provisioning, diet, sex-specific labour division, and the overall level of hardship associated with a particular subsistence strategy.

Acknowledgements

We wish to thank all the indigenous people of African Sahel/Savanah belt who participated in this study. We also wish to thank to Petr Tureček for his most useful advice on statistical analyses and Anna Pilátová for proofreading. This study was supported by Czech Science Foundation projects, reg. no 19-09352S-P505 (VČ) and reg. no 21-10527S (KK and ŠP). We thank two anonymous reviewers for their helpful comments on the previous version of this manuscript.

Data Availability

The dataset and R code is available at https://osf.io/9k3ax/

Authors’ contributions

K.K. developed the study concept and wrote the initial draft. V.Č. collected data in studied populations. V.Č. and K.K. drafted the manuscript. Š.P. digitised landmarks on facial photographs. K.K. performed the analyses and designed the figures. V.Č. and Š.P. reviewed and commented on the manuscript. All authors discussed the results and contributed to the final manuscript.

Tanikawa, C., Akcam, M. O., Gokalp, H., Zere, E. & Takada, K. Population affinity and variation of sexual dimorphism in three-dimensional facial forms: comparisons between Turkish and Japanese populations. Scientific Reports 2021 11:1 11, 1–14 (2021).
Butovskaya, M. L., Rostovtseva, V. v. & Mezentseva, A. A. Facial and body sexual dimorphism are not interconnected in the Maasai. J Physiol Anthropol 41, 3 (2022).
Rostovtseva, V. v., Mezentseva, A. A., Windhager, S. & Butovskaya, M. L. Second-to-fourth digit ratio and facial shape in Buryats of Southern Siberia. Early Hum Dev 149, (2020).
Fiala, V. et al. Facial attractiveness and preference of sexual dimorphism: A comparison across five populations. Evol Hum Sci 3, e38 (2021).
Kleisner, K. et al. How and why patterns of sexual dimorphism in human faces vary across the world. Sci Rep 11, 1–14 (2021).
Pontzer, H., Wood, B. M. & Raichlen, D. A. Hunter-gatherers as models in public health. Obesity Reviews 19, 24–35 (2018).
Armelagos, G. J. & van Gerven, D. P. Sexual dimorphism and human evolution: An overview. J Hum Evol 9, 437–446 (1980).
Cavalli-Sforza, L. L. African Pygmies. African Pygmies. (Academic Press, 1986). doi:10.2307/2803311.
Lee, R. B. The !Kung San: men, women, and work in a foraging society. The Kung San: men, women and work in a foraging society ( Botswana). (Cambridge University Press, 1979).
Marlowe, F. The Hadza : hunter-gatherers of Tanzania. (University of California Press, 2010).
Panter-Brick, C. Sexual division of labor: Energetic and evolutionary scenarios. American Journal of Human Biology 14, 627–640 (2002).
Fischer, B., Grunstra, N. D. S., Zaffarini, E. & Mitteroecker, P. Sex differences in the pelvis did not evolve de novo in modern humans. Nature Ecology & Evolution 2021 5:5 5, 625–630 (2021).
Murail, P., Brůžek, J., Houët, F. & Cunha, E. DSP: A tool for probabilistic sex diagnosis using worldwide variability in hip-bone measurements. http://journals.openedition.org/bmsap 17, 167–176 (2005).
Ruff, C. Sexual dimorphism in human lower limb bone structure: relationship to subsistence strategy and sexual division of labor. J Hum Evol 16, 391–416 (1987).
Ravosa, M. J., Noble, V. E., Hylander, W. L., Johnson, K. R. & Kowalski, E. M. Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. J Hum Evol 38, 667–693 (2000).
Kupczik, K. et al. Masticatory loading and bone adaptation in the supraorbital torus of developing macaques. Am J Phys Anthropol 139, 193–203 (2009).
Claes, P., Hill, H. & Shriver, M. D. Toward DNA-based facial composites: Preliminary results and validation. Forensic Sci Int Genet 13, 208–216 (2014).
Liu, D. et al. Impact of low-frequency coding variants on human facial shape. Scientific Reports 2021 11:1 11, 1–13 (2021).
Stedman, H. H. et al. Myosin gene mutation correlates with anatomical changes in the human lineage. (2004).
Perry, G. H., Verrelli, B. C. & Stone, A. C. Comparative Analyses Reveal a Complex History of Molecular Evolution for Human MYH16. Mol Biol Evol 22, 379–382 (2005).
Warren, J. L. A., de León, M. S. P., Hopkins, W. D. & Zollikofer, C. P. E. Evidence for independent brain and neurocranial reorganization during hominin evolution. Proc Natl Acad Sci U S A 116, 22115–22121 (2019).
Tanikawa, C., Zere, E. & Takada, K. Sexual dimorphism in the facial morphology of adult humans: A three-dimensional analysis. HOMO 67, 23–49 (2016).
Pedersen, J. & Benjaminsen, T. A. One leg or two? Food security and pastoralism in the northern Sahel. Hum Ecol 36, 43–57 (2008).
Braukämper, U. Notes on the origin of Baggara Arab culture with special reference to the Shuwa. in Arabs and Arabic in the Lake Chad region (ed. Ownes, J.) 13–46 (Rüdiger Köppe Verlag, 1994).
Vicente, M. et al. Population history and genetic adaptation of the Fulani nomads: Inferences from genome-wide data and the lactase persistence trait. BMC Genomics 20, 1–12 (2019).
Triska, P. et al. Extensive Admixture and Selective Pressure Across the Sahel Belt. Genome Biol Evol 7, 3484–3495 (2015).
Zeltner, J. C. Histoire des Arabes sur les rives du lac Tchad. (Karthala, 2002).
Zeltner, J. C. Histoire des arabes sur les rives du Tchad. Annales de l’Univ. d’Abidjan, série F: ethnosociologie 2, 109–237 (1970).
Černy, V., Fortes-Lima, C. & Tříska, P. Demographic history and admixture dynamics in African Sahelian populations. Hum Mol Genet 30, R29–R36 (2021).
Priehodová, E. et al. The historical spread of Arabian Pastoralists to the eastern African Sahel evidenced by the lactase persistence −13,915*G allele and mitochondrial DNA. American Journal of Human Biology 29, (2017).
Nováčková, J. et al. Subsistence strategy was the main factor driving population differentiation in the bidirectional corridor of the African Sahel. Am J Phys Anthropol 171, 496–508 (2020).
Černý, V. et al. Genetic Structure of Pastoral and Farmer Populations in the African Sahel. Mol Biol Evol 28, 2491–2500 (2011).
Bučková, J., Černý, V. & Novelletto, A. Multiple and differentiated contributions to the male gene pool of pastoral and farmer populations of the African Sahel. Am J Phys Anthropol 151, 10–21 (2013).
Cerezo, M., Černý, V., Carracedo, Á. & Salas, A. New Insights into the Lake Chad Basin Population Structure Revealed by High-Throughput Genotyping of Mitochondrial DNA Coding SNPs. PLoS One 6, e18682 (2011).
Turner, M. D. & Schlecht, E. Livestock mobility in sub-Saharan Africa: A critical review. Pastoralism 9, 1–15 (2019).
Homewood, K. Ecology of African Pastoralist Societies. (Ohio University Press, 2009).
Swift, J. Sahelian Pastoralists: Underdevelopment, Desertification, and Famine. Annu Rev Anthropol 6, 457–478 (1977).
Ouédraogo, K., Zaré, A., Korbéogo, G., Ouédraogo, O. & Linstädter, A. Resilience strategies of West African pastoralists in response to scarce forage resources. Pastoralism 11, 1–14 (2021).
Little, M. A. Human biology, health, and ecology of nomadic Turkana pastoralists. in Human Biology of Pastoral Populations (eds. Leonard, W. R. & Crawford, M. H.) 151–182 (Cambridge University Press, 2002).
Priehodová, E. et al. Sahelian pastoralism from the perspective of variants associated with lactase persistence. Am J Phys Anthropol 173, 423–436 (2020).
Kleisner, K., Pokorný, Š., Čížková, M., Froment, A. & Černý, V. Nomadic pastoralists and sedentary farmers of the Sahel/Savannah Belt of Africa in the light of geometric morphometrics based on facial portraits. Am J Phys Anthropol 169, 632–645 (2019).
Galvin, K. A., Beeton, T. A., Boone, R. B. & BurnSilver, S. B. Nutritional Status of Maasai Pastoralists under Change. Hum Ecol 43, 411–424 (2015).
de Haan, C., Dubern, E., Garancher, B. & Quintero, C. Pastoralism Development in the Sahel A Road to Stability? (nternational Bank for Reconstruction and Development / The World Bank, 2016).
Raynaut, C. & Delville, P. L. Un espace partagé : Complémentarité et concurrence des usages. in Sahels Diversité et dynamiques des relations sociétés-nature (ed. Raynaut, C.) 143–174 (Karthala, 1997).
Adams, D. C. & Otárola‐Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4, 393–399 (2013).
Mardia, K. v, Bookstein, F. L. & Moreton, I. J. Statistical assessment of bilateral symmetry of shapes. Biometrika 285–300 (2000).
Bookstein, F. L. Principal Warps: Thin-Plate Splines and the Decomposition of Deformations. IEEE Trans Pattern Anal Mach Intell 11, 567–585 (1989).
Baken, E. K., Collyer, M. L., Kaliontzopoulou, A. & Adams, D. C. geomorph v4.0 and gmShiny: Enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Methods Ecol Evol 12, 2355–2363 (2021).
Collyer, M. L. & Adams, D. C. {RRPP}: Linear Model Evaluation with Randomized Residuals in a Permutation Procedure, R package version 0.4.0. Preprint at https://cran.r-project.org/package=RRPP (2019).
Collyer, M. L. & Adams, D. C. Phenotypic trajectory analysis: comparison of shape change patterns in evolution and ecology. Hystrix, the Italian Journal of Mammalogy 24, 75–83 (2013).
Frayer, D. W. Sexual dimorphism and cultural evolution in the Late Pleistocene and Holocene of Europe. J Hum Evol 9, 399–415 (1980).
Brace, C. L. & Ryan, A. S. Sexual dimorphism and human tooth size differences. J Hum Evol 9, 417–435 (1980).
Wolfe, L. D. & Patrick Gray, J. Subsistence practices and human sexual dimorphism of stature. J Hum Evol 11, 575–580 (1982).
Kleisner, K. et al. How and why patterns of sexual dimorphism in human faces vary across the world. (2020) doi:10.31234/osf.io/7vdmb.
Scott, I., Swami, V., Josephson, S. C. & Penton-Voak, I. S. Context-dependent preferences for facial dimorphism in a rural Malaysian population. Evolution and Human behavior 29, 289–296 (2008).
Scott, I. M. et al. Human preferences for sexually dimorphic faces may be evolutionarily novel. Proceedings of the National Academy of Sciences (2014) doi:10.1073/pnas.1409643111.
Scott, I. M., Pound, N., Stephen, I. D., Clark, A. P. & Penton-Voak, I. S. Does masculinity matter? The contribution of masculine face shape to male attractiveness in humans. PLoS One 5, e13585 (2010).
Marcinkowska, U. M. et al. Cross-cultural variation in men’s preference for sexual dimorphism in women’s faces. Biol Lett 10, 4–7 (2014).
Johnston, V. S., Hagel, R., Franklin, M., Fink, B. & Grammer, K. Male facial attractiveness Evidence for hormone-mediated adaptive design Victor. Evolution and Human Behavior 22, 251–267 (2001).
Lyons, M., Marcinkowska, U., Moisey, V. & Harrison, N. The effects of resource availability and relationship status on women’s preference for facial masculinity in men: An eye-tracking study. Pers Individ Dif 95, 25–28 (2016).
Marcinkowska, U. M., Jasienska, G. & Prokop, P. A Comparison of Masculinity Facial Preference Among Naturally Cycling, Pregnant, Lactating, and Post-Menopausal Women. Arch Sex Behav 47, 1367–1374 (2018).
Moore, F. R. et al. Cross-cultural variation in women’s preferences for cues to sex-and stress-hormones in the male face. Biol Lett 9, 20130050 (2013).
Marcinkowska, U. M. et al. Women’s preferences for men’s facial masculinity are strongest under favorable ecological conditions. Sci Rep 9, 1–10 (2019).
Little, A. C., Burriss, R. P., Petrie, M., Jones, B. C. & Roberts, S. C. Oral contraceptive use in women changes preferences for male facial masculinity and is associated with partner facial masculinity. Psychoneuroendocrinology 38, 1777–1785 (2013).
Coetzee, V. & Perrett, D. I. African and Caucasian body ideals in South Africa and the United States. Eat Behav 12, 72–74 (2011).
Schneider, T. M., Hecht, H. & Carbon, C. C. Judging body weight from faces: The height-weight illusion. Perception 41, 121–124 (2012).
Coetzee, V., Perrett, D. I. & Stephen, I. D. Facial adiposity: A cue to health? Perception 38, 1700–1711 (2009).
Holzleitner, I. J. et al. Men’s facial masculinity: When (body) size matters. Perception 43, 1191–1202 (2014).
Zaidi, A. A. et al. Facial masculinity does not appear to be a condition-dependent male ornament and does not reflect MHC heterozygosity in humans. Proc Natl Acad Sci U S A 116, 1633–1638 (2019).
Krams, I. A. et al. Body height affects the strength of immune response in young men, but not young women. Sci Rep 4, 6223 (2014).
Shepperd, J. A. & Strathman, A. J. Attractiveness and Height. Pers Soc Psychol Bull 15, 617–627 (1989).
Stulp, G. & Barrett, L. Evolutionary perspectives on human height variation. Biological Reviews 91, 206–234 (2016).
Pierce, C. A. Body height and romantic attraction: A meta-analytic test of the male-taller norm. Soc Behav Pers 24, 143–150 (1996).
Marlowe, F. W. Mate preferences among Hadza hunter-gatherers. Human Nature 15, 365–376 (2004).
Sear, R. & Marlowe, F. W. How universal are human mate choices? Size does not matter when Hadza foragers are choosing a mate. Biol Lett 5, 606–609 (2009).
Sorokowski, P., Sorokowska, A., Fink, B. & Mberira, M. Variable preferences for sexual dimorphism in stature (SDS) might not be universal: Data from a semi-nomad population (Himba) in Namibia. J Cross Cult Psychol 43, 32–37 (2012).
Lidborg, L. H., Cross, C. P. & Boothroyd, L. G. A meta-analysis of the association between male dimorphism and fitness outcomes in humans. Elife 11, (2022).
Ranciaro, A. et al. Genetic Origins of Lactase Persistence and the Spread of Pastoralism in Africa. The American Journal of Human Genetics 94, 496–510 (2014).
Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nature Genetics 2006 39:1 39, 31–40 (2006).
Sabbagh, A., Darlu, P., Crouau-Roy, B. & Poloni, E. S. Arylamine N-Acetyltransferase 2 (NAT2) Genetic Diversity and Traditional Subsistence: A Worldwide Population Survey. PLoS One 6, e18507 (2011).
Hernández-González, O., Herrera-Vargas, D. J., Martínez-Leija, M. E., Zavala-Reyes, D. & Portales-Pérez, D. P. The role of arylamine N-acetyltransferases in chronic degenerative diseases: Their possible function in the immune system. Biochim Biophys Acta Mol Cell Res 1869, (2022).
Podgorná, E. et al. Variation in NAT2 acetylation phenotypes is associated with differences in food-producing subsistence modes and ecoregions in Africa. BMC Evol Biol 15, 1–20 (2015).
Čížková, M. et al. Genetic structure of the western and eastern African Sahel/Savannah belt and the role of nomadic pastoralists as inferred from the variation of D-loop mitochondrial DNA sequences. Hum Biol 89, 281–302 (2017).
Verdu, P. et al. Sociocultural Behavior, Sex-Biased Admixture, and Effective Population Sizes in Central African Pygmies and Non-Pygmies. Mol Biol Evol 30, 918–937 (2013).
Wilson, M. L., Miller, C. M. & Crouse, K. N. Humans as a model species for sexual selection research. Proceedings of the Royal Society B: Biological Sciences 284, (2017).

No competing interests reported.

Supplementarymaterial.docx

Download PDF

Journal Publication

published 28 Oct, 2023

Read the published version in American Journal of Human Biology →

Version 1

posted

You are reading this latest preprint version

Sexually dimorphic traits are associated with subsistence strategy in African faces from the Sahel/Savannah belt

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Material And Methods

The subjects and acquisition of facial photographs

Geometric morphometrics

Statistical analysis

Results

Discussion

Conclusions

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1