The evolution of human skin coloration

Skin color is one of the most conspicuous ways in which humans vary and has been widely used to define human races. Here we present new evidence indicating that variations in skin color are adaptive, and are related to the regulation of ultraviolet (UV) radiation penetration in the integument and its direct and indirect effects on fitness. Using remotely sensed data on UV radiation levels, hypotheses concerning
the distribution of the skin colors of indigenous peoples relative to UV levels were tested quantitatively in this study for the first time.

The major results of this study are: (1) skin reflectance is strongly correlated with absolute latitude and UV radiation levels. The highest correlation between skin reflectance and UV levels was observed at 545 nm, near the absorption maximum for oxyhemoglobin, suggesting that the main role of melanin pigmentation in humans is regulation of the effects of UV radiation on the contents of cutaneous blood vessels located in the dermis. (2) Predicted skin reflectances deviated little from observed values. (3) In all populations for which skin reflectance data were available for males and females, females were found to be lighter skinned than males. (4) The clinal gradation of skin coloration observed among indigenous peoples is correlated with UV radiation levels and represents a compromise solution to the conflicting physiological requirements of photoprotection and vitamin D synthesis.

The earliest members of the hominid lineage probably had a mostly unpigmented or lightly pigmented integument covered with dark black hair, similar to that of the modern chimpanzee. The evolution of a naked, darkly pigmented integument occurred early in the evolution of the genus Homo. A dark epidermis protected sweat glands from UV-induced injury, thus insuring the integrity of somatic thermoregulation. Of greater significance to individual reproductive success was that highly melanized skin protected against UV-induced photolysis of folate (Branda & Eaton, 1978, Science 201, 625–626; Jablonski, 1992, Proc. Australas. Soc. Hum. Biol. 5, 455–462, 1999, Med. Hypotheses 52, 581–582), a metabolite essential for normal development of the embryonic neural tube (Bower & Stanley, 1989, The Medical Journal of Australia 150, 613–619; Medical Research Council Vitamin Research Group, 1991, The Lancet 338, 31–37) and spermatogenesis (Cosentino et al., 1990, Proc. Natn. Acad. Sci. U.S.A. 87, 1431–1435; Mathur et al., 1977, Fertility Sterility 28, 1356–1360).

As hominids migrated outside of the tropics, varying degrees of depigmentation evolved in order to permit UVB-induced synthesis of pre-vitamin D3. The lighter color of female skin may be required to permit synthesis of the relatively higher amounts of vitamin D3 necessary during pregnancy and lactation.

Skin coloration in humans is adaptive and labile. Skin pigmentation levels have changed more than once in human evolution. Because of this, skin coloration is of no value in determining phylogenetic relationships among modern human groups.

Figure 1. The potential for synthesis of previtamin D3 in lightly pigmented human skin computed from annual average UVMED. The highest annual values for UVMED are shown in light violet, with incrementally lower values in dark violet, then in light to dark shades of blue, orange, green and gray (64 classes). White denotes areas for which no UVMED data exist. Mercator projection. In the tropics, the zone of adequate UV radiation throughout the year (Zone 1) is delimited by bold black lines. Light stippling indicates Zone 2, in which there is not suffcient UV radiation during at least one month of the year to produce previtamin D3 in human skin. Zone 3, in which there is not suffcient UV radiation for previtamin D3 synthesis on average for the whole year, is indicated by heavy stippling.



Figure 2. A comparison of the estimated areas in which annual UVMED is not sufficient, averaged over the year, to catalyze previtamin D3 synthesis in lightly, moderately and highly melanized skin. All zones were defined by the values for previtamin D3 synthesis potential presented in Table 2. Widely spaced oblique hachure covers the northernmost region of the Northern Hemisphere in which there is not sufficient UV radiation, averaged over the entire year, to catalyze the formation of previtamin D3 in lightly pigmented (Type IIIa) human skin (Zone 3 from Figure 1). Narrowly spaced oblique hachure denotes the area, in addition to that shown by widely spaced oblique hachure, in which there is not sufficient UV radiation to catalyze the formation of previtamin D3 in moderately melanized (Type V) skin. The large circum-Equatorial area denoted by stippling covers the area, in addition to the previous two, in which there is not sufficient UV radiation averaged over the entire year to catalyze the formation of previtamin D3 in highly melanized (Type VI)
skin.

Figure 3. Predicted shading of skin colors for indigenous humans based on the results of a linear regression model in which skin reflectance (at 685 nm) for indigenous peoples in both hemispheres was allowed to respond to annual average UVMED for both hemispheres. The predicted skin reflectance values were first divided into 50 equal intervals and then graphically represented in gray shades ranging from darkest gray (greatest melanization) to lightest gray (least melanization). Darker shades of gray represent a higher degree of skin melanization and do not represent actual predicted skin colors.

Figure 4. Gradation of skin colors for known indigenous human populations, represented by shading from darkest to lightest gray (greatest to least melanization, as in Figure 3), based on observed skin reflectances at 685 nm reported in Table 6.

Conclusions
The results presented here demonstrate that skin coloration in humans is highly adaptive and has evolved to accommodate the physiological needs of humans as they have dispersed to regions of widely varying annual UVMED. The dual selective pressures of photoprotection and vitamin D3 synthesis have created two clines of skin pigmentation. The first cline, from the equator to the poles, is defined by the significantly greater need for photoprotection at the equator in particular and within the tropics in general. Deeply melanized skin protects against folate photolysis and helps to prevent UV-induced injury to sweat glands(and subsequent disruption of thermoregulation). The second cline, from approximately 30N to the North Pole, is defined by the greater need in high latitudes to accommodate as much previtamin D3 synthesis as possible in areas of low annual UVMED. Humans inhabiting regionsat the intersection of these clines demonstrate a potential for developing varying degrees of facultative pigmentation (tanning) (Quevedo et al., 1975). Moderately melanized skin would appear to be at risk of vitamin D3 deficiency and rickets under conditions where UV radiation is restricted as a result of latitude, cultural practices or both.

The results of this study suggest that skin pigmentation is relatively labile, and that adaptations to local UVMED conditions can occur over relatively short periods of geological time. Thus, it is likely that some human lineages through time may have gone through alternating periods of depigmentation and pigmentation (or vice versa) as they moved from one UVMED regime to another. As the pace of human migrations has quickened in recent centuries, more and more populations are finding themselves living under UV irradiation regimes to which they are inherently poorly adapted (e.g., the English who settled in Australia in the nineteenth and twentieth centuries, and the Indians and Pakistanis who have moved to northern England in recent decades), with major public health consequences (Kaidbey et al., 1979; Henderson et al., 1987). Cultural practices such as sun-bathing and purdah have in some cases exacerbated these conditions and mitigated others. Because of its high degree of responsiveness to environmental conditions, skin pigmentation is of no value in assessing the phylogenetic relationships between human groups.