Evolution of long scalp hair in humans

Abstract

The ability to grow long scalp hair is a distinct human characteristic. It probably originally evolved to aid in cooling the sun-exposed head, although the genetic determinants of long hair are largely unknown. Despite ancestral variations in hair growth, long scalp hair is common to all extant human populations, which suggests its emergence before or concurrently with the emergence of anatomically modern humans (AMHs), approximately 300 000 years ago. Long scalp hair in AMHs was also a trait that was selected because it conveyed essential signals related to an individual's age, sexual maturity, health and social status. Biologically, hair length is primarily determined by the amount of time that a hair follicle spends in the active growth phase (anagen). While anagen duration is typically tightly regulated in most mammals, the inherent ability of a hair follicle to continuously recruit new dividing progenitors to its base, where hair fibre is generated, theoretically removes limits on maximal anagen duration. We propose a model wherein hair cycle progression into and out of anagen is regulated by evolutionary malleable molecular checkpoints. Several animal species and domesticated animal breeds display long body hair, which suggests that extremely long scalp hair in humans emerged via attenuation of an existing out-of-anagen checkpoint mechanism rather than via a newly evolved molecular programme. Studying congenital and somatic mosaicism conditions featuring altered hair length could potentially unveil the currently unknown molecular basis underlying this human trait.

Figure 1

Evolution of scalp hair traits in anatomically modern humans (AMHs). (a) AMHs evolved in Africa approximately 300 thousand years ago (kya). African AMH populations were genetically diverse and broadly featured long, tightly curled scalp hair, which was styled for visual communication. Upon dispersal from Africa starting approximately 200 kya (red arrows), AMHs had contact with and experienced genetic admixture from archaic humans (the area showing the Neanderthals’ range is shaded in yellow). From Western Asia, humans dispersed into Europe, Oceania, Central and Eastern Asia, and then into North and South America (around 25 kya). Long scalp hair remained a universal anatomical feature in all non-African populations, while hair curliness and thickness further diversified. Dispersal history of AMHs is adopted from Nielsen et al. Further information on the timeline of hominin evolution is provided in Figure S1 (see Supporting Information). The background image represents an approximate world map during Last Glacial Maximum (LGM), approximately 20 kya. (b) The proposed primary role of long, tightly curled scalp hair in AMHs. The Equatorial Africa region represented the original ecological niche of AMHs and was characterized by high-intensity solar radiation. The human head was exposed to direct sunlight, posing a risk of overheating which could affect the brain. To counter overheating, increased sweat gland density enabled active heat loss via perspiration. However, perspiration results in significant loss of water and electrolytes (left). Evolution of long scalp hair enabled physical head shielding, reducing direct sunlight exposure of the skin and the required amount of perspiration (centre and right). However, long straight hair is prone to losing volume when wet, which decreases its head-shielding capacity (right), whereas long, tightly curled hair has better water resistance and maintains high volume, thus offering robust head-shielding efficacy (centre). Long, tightly curled hair evolved as the ancestral scalp hair state in AMHs.

Figure 2

Long scalp hair and hairpieces in prehistoric art and during early history. (a) Venus of Willendorf from modern day Austria dating from approximately 24–26 thousand years ago (kya). The head features prominent covering, which may represent either natural curly hair or a hairpiece (arrow). (b) Venus of Brassempouy from modern day France dating from approximately 23–25 kya. The head features prominent covering, which might represent braided long scalp hair or a headpiece (arrow). (c) Gwion Gwion rock painting from modern day Western Australia dating from approximately 12 kya. It depicts two human figures with likely long, styled scalp hair (arrows). (d) Egyptian mummy of Tiye, the great royal wife of pharaoh Amenhotep III (18th dynasty; year of death 1338 Bc). It features natural long, wavy scalp hair (arrow). (e) Princess Nofret from the fourth dynasty of Ancient Egypt (approximately 2490 Bc). The head is covered with a styled wig (arrow) placed over natural hair, which is visible above the forehead and straight in appearance (arrowhead). (f) Painted bas-relief from tomb QV44, depicting prince Khaemwaset, son of pharaoh Rameses III (20th dynasty; approximately 1250 Bc). The head features a hairstyle typical of children in Ancient Egypt at that time, namely long, braided hair on a side and shaved surrounding skin.

Figure 3

Hair follicle morphology, cellular dynamics and key regulatory events across hair growth cycle. (a) Schematic drawing of the hair growth cycle. Bulge and secondary hair germ epithelial hair follicle (HF) stem cells (eHFSCs) are quiescent during telogen. They transiently activate during anagen onset to regenerate the lower HF segment. During the catagen phase, the lower HF segment regresses, driven by apoptosis. Key HF cell types and compartments are annotated and colour-coded. (b) Hair growth cycle checkpoint model. The growth cycle can be conceptualized into two phases, anagen (green) and catagen/telogen (red). The progression of the HF through these phases is controlled at checkpoints C and A, which regulate transition from anagen to catagen/telogen and from catagen/telogen to anagen, respectively. The lower portion of the figure depicts hypothetical results of hair growth under high and low checkpoint C probabilities. The results are depicted as vectors, whose length represents resulting hair fibre (short for high checkpoint C probability and extremely long for low probability). (c) Cellular dynamics of eHFSCs upon anagen initiation and progression. Primed secondary hair germ eHFSCs activate during anagen subphase I, while bulge eHFSCs activate with a delay during anagen II/III. eHFSCs proliferate rarely during other phases. (d) Cellular dynamics in the anagen HF bulb under continuous progenitor recruitment model. Germinative matrix cells proliferate and subsequently differentiate into trichocytes (short blue arrows) to support continuous hair elongation and that of associated sheaths (long white arrows). Outer root sheath and lower proximal cup cells have progenitor properties and can continuously migrate towards the hair matrix to, in principle, replenish ‘exhausted’ germinative cells. This ‘resupply’ mechanism (long blue arrow) endows anagen HFs with the potential for an extended growth.

Figure 4

Hair length flexibility in animals and in humans upon conditions with altered hair growth. (a–h) Examples of animal species with naturally occurring long hair. (a) Grey seals (Halichoerus grypus) feature long vibrissa hairs that form a sensory ‘sphere’ around the snout. (b) Malayan porcupines (Hystrix brachyura) feature very long dorsal quill hairs. (c) Adult male lions (Panthera leo) feature long mane hairs. (d) Muskoxes (Ovibos moschatus) grow long pelage hair, which drapes over the body. (e–h) Examples of primates with long hair. (e) Adult male Hamadryas baboons (Papio hamadryas) grow long facial and body hair. (f) Emperor tamarins (Saguinus imperator) grow long facial hair. (g) Mantled guerezas (Colobus guereza) grow distinctly coloured long dorsal body hair. (h) Adult male Bornean orangutans (Pongo pygmaeus) grow very long body hair, especially in captivity. (i–l) Examples of domesticated animal breeds with long hair: (i) Ragdoll cat (Felis catus), (j) Lhasa Apso and (k) Bearded Collie dogs (Canis lupus familiaris), and (l) Highland cattle (Bos taurus). (m) Head of an old stump-tailed macaque (Macaca arctoides) displaying frontal hair loss. (n) Example of short anagen syndrome in patient carrying heterozygous WNT10A variant. Scalp hair is sparse and short, frontal hairline is high. (o) Example of a hairy melanocytic naevus featuring long, thick and darkly pigmented hair.