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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 125:292–302 (2004)

Geographic Distribution of Environmental Factors Influencing Human Skin Coloration

George Chaplin*

Department of Anthropology, California Academy of Sciences, San Francisco, California 94118

KEY WORDS

photobiology; race; GIS

integument; spectrometry; reflectometry; pigmentation; sunlight; adaptation;

ABSTRACT Skin coloration in indigenous peoples is strongly related to levels of ultraviolet radiation (UVR). In this study, the relationships of skin reflectance to seasonal UVR levels and other environmental variables were inves- tigated, with the aim of determining which variables con- tributed most significantly to skin reflectance. The UVR data recorded by satellite were combined with environ- mental variables and data on human skin reflectance in a geographic information system (GIS). These were then analyzed visually and statistically through exploratory data analysis, correlation analysis, principal components analysis, least-squares regression analysis, and nonlinear

techniques. The main finding of this study was that the evolution of skin reflectance could be almost fully modeled as a linear effect of UVR in the autumn alone. This linear model needs only minor modification, by the introduction of terms for the maximum amount of UVR, and for sum- mer precipitation and winter precipitation, to account for almost all the variation in skin reflectance. A further significant finding was that the effect of summer UVR seems to reach a threshold beyond which further adapta- tion is difficult. Am J Phys Anthropol 125:292–302, 2004.

© 2004 Wiley-Liss, Inc.

This paper presents an investigation of the spe- cific nature of environmental influences on the evo- lution of human skin coloration. It builds on previ- ous research (Jablonski and Chaplin, 2000) in which a clear causal relationship between average annual ultraviolet radiation (UVR) and skin reflectance was established.

PREVIOUS RESEARCH ON GLOBAL DISTRIBUTION OF ENVIRONMENTAL FACTORS

Few workers have looked systematically at the environmental factors identified as possible influ- ences on skin color. Most have used latitude as a surrogate for UVR because it has a strong correla- tion with skin color, with an r-value of around 0.8 (Relethford, 1997; Roberts, 1977; Roberts and Kahlon, 1976; Tasa et al., 1985). Latitude is a poor surrogate for UVR because other environmental variables are correlated with it. Further, the corre- lation between UVR and latitude will be different between the hemispheres due to orbital effects on solar intensity (Chaplin and Jablonski, 1998; Relethford, 1997). The first use of direct measure- ments of UVR collected using a satellite (Jablonski and Chaplin, 2000) showed the highest correlation to annual average UVR and skin reflectance at r- values above 0.95, but no other environmental fac- tors were taken into account. Walter (1958) was the first to use an estimate of UVR to demonstrate a correlation between UVR and skin color. He obtained his estimate by calculating UVR at the Equator and correcting for latitude,

© 2004 WILEY-LISS, INC.

clouds, moisture, vegetation, and albedo. He then used statistical and visual map comparisons to con- clude that there was a correlation of UVR with skin color, and that it was modified by selection for ther- moregulation. Roberts and Kahlon (1976) showed that, in addi- tion to the dominance of latitude, there were also correlations of skin color with minimum, mean, and maximum temperature, with minimum and maxi- mum humidity, and with altitude. They combined these variables in a multiple additive regression. However, they posited no direct effect of these vari- ables on skin color other than as modifiers for ground UVR estimation and in thermoregulation. Roberts (1977) drew similar conclusions to Walter (1958) and expanded them in a review. The skin measurements Roberts and Kahlon (1976) used were assumed to be representative of the geographic area where they were measured, and not of the whole of the area that the subjects occupied. The variables of Roberts and Kahlon (1976) were more of a point-by-point estimate than an area-wide average

*Correspondence to: George Chaplin, Department of Anthropology, California Academy of Sciences, Golden Gate Park, San Francisco, CA 94118. E-mail: gchaplin@calacademy.org

Received 10 April 2002; accepted 3 January 2003.

DOI 10.1002/ajpa.10263 Published online 4 May 2004 in Wiley InterScience (www. interscience.wiley.com).

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(the only practical solution prior to the use of a geographic information system (GIS)). This study sought to replicate the work of Roberts and Kahlon (1976), using directly measured UVR instead of latitude. UVR and other environmental variables were taken for the whole of the area that a particular human population occupied. This ap- proach was impossible before the advent of GIS. In this study, the relationship of environmental effects variables to skin color reflectance was exam- ined. Prior to this study, important variations in environmental factors, such as the relative impor- tance of maximum UVR and minimum UVR, the temporal evenness of UVR dose, and the seasonal aspect to the distribution of UVR throughout the year, had not been explored in relation to skin color.

HYPOTHESES TESTED

Several environmental factors, especially those related to UVR dosage and intensity, have been proposed as being causally related. First, are these hypotheses concerned with direct UVR effects and to disease or trauma processes and skin coloration? Previous researchers proposed that maximum UVR, average UVR, or temporal patterns of UVR dose are related to incidents of sunburning. Radiation-in- duced damage is known to cause cancer (melanoma and basal- and squamous-cell carcinoma; Buzzell, 1993; Kollias et al., 1991; Longstreth et al., 1998; Potten et al., 1993; Zihlman and Cohn, 1988) and to damage sweat glands (Daniels, 1964; Pandolf et al., 1992). Both UVB and long-wave UVR (UVA) can cause deleterious effects in the skin, with those from UVA being mediated by reactive oxygen species (Cleaver and Mitchell, 2000; Roberts, 1977) This led to formulation of the hypothesis that reduced skin reflectance is mediated directly by exposure to UVR through reduced reproductive fitness. Another cause of reduced skin reflectance, particularly in the tissue (blue) reflectance range, is the thickening of the stratum corneum caused directly by UVR (Kollias et al., 1991). Second are hypotheses that suggest that UVR me- diates the body’s production and storage of vital nutrients. For example, a highly seasonal distribu- tion of UVR throughout the year (especially where winter levels are greatly reduced or nonexistent) causes problems for vitamin D production and stor- age (Holick, 1981; Loomis, 1967; Murray, 1934; Jab- lonski and Chaplin, 2000). Some vital nutrients stored in the body are subject to photolysis. Folate may be destroyed by strong summer levels of UVA, and in areas with sunny winters that have moderate to high levels of long-wave UVR, both folate and vitamin D are destroyed (Jablonski, 1992, 1999; Jab- lonski and Chaplin, 2000; Jones et al., 1998; Webb and Holick, 1988). These theories led to formulation of the hypothesis that metabolic processes related to direct solar radiation are responsible for variation of fitness, leading to a correlation between skin reflec- tance and UVR.

Third are hypotheses that involve non-UVR agen- cies, such as forest cover, altitude, temperature, and precipitation. These variables have been considered in theories of skin coloration and were included in this study. It was suggested that the intensity of melanin pigmentation is related to the need for cam- ouflage in forest environments (Cowles, 1959). A number of theories revolve around thermoregula- tion (Baker, 1958; Hamilton and Heppner, 1967; Razi et al., 1980) or the prevention of cold injury (Candler and Ivey, 1997; Post et al., 1975; Steeg- mann, 1967; Taylor, 1992). Precipitation was in- cluded because Gloger’s rule states that warm- blooded animals living in warm and humid places are more heavily pigmented than those in cool, dry areas. Precipitation may also be indicative of the need for shelter-seeking and cultural modification of the UVR regime, leading to pleiotropic decline in skin coloration (Brace, 1963; Daniels, 1964; Deol, 1975). This led to formulation of the hypothesis that variables other than direct UVR are responsible for skin reflectance and are only correlated to UVR or latitude by solar-driven processes such as vegeta- tion, temperature, and precipitation.

MATERIALS

Skin reflectance data

The skin reflectance data set used in this study was essentially the same as that of Jablonski and Chaplin (2000), but with a few new data points added (see Appendix). The database comprises sam- ples for reflectance at 425 nm (blue filter), 545 nm (green filter), and 685 nm (red filter), at a site on the upper inner arm.

Environmental data

The UVR data used in this study represent the relative daily areal exposure to the ultraviolet min- imum erythemal dose (UVMED), i.e., the amount of UVR effective in causing a barely perceptible red- dening of light skin. The values for UVMED used in this study were derived from readings taken by the NASA total ozone mapping spectrometer (TOMS) that was flown aboard the Nimbus-7 satellite be- tween 1978 –1993 (Herman and Celarier, 1996). In measuring UVR strength, all attenuating influences (humidity, rainfall, temperature, or elevation) were already discounted, so that any effect that these variables have, as modeled in this study, was the result of their own action rather than how they were affecting UVR transmittance. The treatment of TOMS data was described in Jablonski and Chaplin (2000). From the NASA TOMS data set, the follow- ing UVMED readings were derived: annual mean for maximum, minimum, and range, and seasonal average for winter, spring, summer, and autumn. Data for global environmental variables were taken from the unified data set, ArcAtlas: Our Earth (ESRI, 1996). These data were provided at scales of 25 million to 1, and 10 million to 1, for selected

294

G. CHAPLIN

places. The following environmental data were used:

1) total solar radiation measured in millijoules (mJ) per square mile; 2) air temperature readings for yearly average, and for January and July measured in degrees Celsius; 3) average length of the frost-free period, defined as number of days per year; 4) total number of days with snow on the ground (in days per year); 5) average amount of all precipitation reaching the ground (yearly average, and for months of January and July, all measured in millimeters); 6) reconstructed ground-cover polygons in the Arc- World data, for the cover type as it existed before human disturbance (Ground cover was classified as desert, forest, or other. Where an area had more than one ground-cover class type, it was assigned the majority type, or where it was judged that there was not a clear majority, it was designated as other.); and 7) a classification of land surface relief in the following terms: glaciers, high mountains, high plains, low mountains, low plains, middle moun- tains, plateau, and tablelands. In order that environmental variables be explored for both hemispheres at the same time, it was de- cided to join them by seasons, which are offset by 6 months. To do this, each corresponding month was joined together, e.g., April, the first month of South- ern Hemisphere autumn, was joined to the Northern Hemisphere’s October. These were then averaged over 3-month periods and renamed for their corre- sponding season.

METHODS

Statistical treatment

For each skin reflectance sampled area, the cells corresponding to it were extracted from the data- base by spatial join or overlay. These data were placed into the S-Plus statistical data package for further analysis (MathSoft, 1999).

Exploratory data analysis

The variables were studied for normality, kurto- sis, and skew. Exploratory data analysis was con- ducted to detect and remove outliers and data anom- alies.

Correlation

The skin reflectance data set was used to estimate the new variables, named Melanin Reflectance, Tis- sue Reflectance, and Blood Reflectance. They were so named because these three main light-absorbing pigments have peaks in the red, blue, and green wavelengths, respectively. These variables were de- rived, respectively, from the readings of either the Evans Electroselenium Company Ltd. (EEL) or Pho- tovolt reflectometers for the following pairs of reflec- tance filters: the “E685.609-P670.Red” red pair, the “E425.601-P420.Blue” blue pair, and the “E545.605- P525.Green” green pair. The correlations within data were checked. The correlation table included the raw values and the

trimmed and grouped data to show that this data selection method had little effect on the overall pat- tern of variation within the data.

Principal components analysis

It was first hoped to use stepwise regression to identify the variables that influenced skin coloration in the manner of Roberts and Kahlon (1976). How- ever, the existence of a very high amount of col- linearity in the variables made stepwise regression inadvisable (Johnston, 1978). Therefore, it was nec- essary to use principal components analysis (PCA) as a first investigation, because this has the advan- tage of rewriting the data into uncorrelated compo- nents (Johnston, 1978). A PCA was run using the correlation matrix, because PCA is sensitive to dif- ferent scales within the data if the covariance ma- trix is used.

Data reduction

PCA and the raw correlation readings were used to identify a subset of variables that could explain a large majority of the variation, so that the relation- ship could be further analyzed using linear and non- linear regression techniques. This subset of terms had equal explanatory power, but was much less collinear.

Regression analysis

First, the identified subset of terms was used in a stepwise regression, using a fully specified model to see if there were any significant interactions be- tween variables. Using this method, UVR range was eliminated from further investigation. Winter precipitation was only a minor component in two analyses, but was retained as it still raised the coefficient of determi- nation (r 2 ) slightly. Least squares regression was run, using the four variables identified by data-reduction techniques (UVR Autumn, UVR Winter, Winter Precipitation, and Summer Precipitation).

Spatial bias and autocorrelation

To test if there was significant error introduced by treating geographic variables as independent, in the light of possible spatial autocorrelation in data con- nected to geography (Cressie, 1993), the residuals of the regression were inspected using correlation and regression against both latitude and longitude sep- arately, and latitude and longitude together. The previous test was useful for checking that there was no difference between hemispheres in skin reflec- tance response, as suggested by Relethford (1997). To test this premise further, t-tests were performed on the residuals of the regression and on the data of the two hemispheres, but with the span of latitudes restricted to be the same ( 25°), so that the samples were not different in the two hemispheres (Chaplin and Jablonski, 1998).

ENVIRONMENT AND HUMAN SKIN COLORATION

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Nonlinear investigation

Further, graphical techniques were run to inves- tigate the relationships as identified in the final regression model. The nonlinear techniques con- sisted of local regression, (loess) regression, and spline fitting. Smoothing splines that minimize a penalized residual sum of squares was done using four degrees of freedom (d.f.), because this will not force oversmoothing (S-Plus, 2000).

Analysis of categorical variables

To investigate categorical variables (relief and land-cover type), boxplot techniques were used, and an analysis of variance was performed. The latter looked for variation that could be further explained by inclusion of these categorical variables.

Prediction from final regression model

The final regression model was used to predict skin reflectance for each color filter. These predicted skin colors were then mapped. The colors of the map were produced from the multiple regression formu- lae for each color filter. This map was, in effect, an intersection of all the input maps. The legend was created by assigning a color to each unique combi- nation derived from the values of the red, green, and blue (RGB) filters, to derive a RGB color value using the GIS programming language. These colors are realistic approximations of the true color of skin, within the limits of the color space of the particular medium in which it is viewed. The large number of features and color combina- tions meant that this map needed generalization for visualization of any trends in predicted skin color. It was generalized as follows: cells were first dissolved until they had unique combinations of red, green, and blue values. Then the lowest and highest values in the distribution tail, that had only a few cells each, were unioned into a single shape. Finally, shapes that were almost identical in color were merged with their neighbors to further reduce the number of shapes. By this method, the number of shapes was reduced to just 17 multipart shapes. The generalization sought to reach a balance between equal area representation and equal interval repre- sentation. The colors in the legend are also the ac- tual skin colors as defined above. This map was suitable for visualization techniques (Cleveland, 1993), but not for statistical analysis.

RESULTS

Exploratory data analysis

Outliers that were detected were examined, and where their explanation could be understood in terms of migration, genetic admixture, or incorrect placement on the map, they were removed from further analysis. These consisted of very few cases. The first were the Ammassalimiut (Inuit from Greenland) and Yemeni Jews; these were removed

because these populations had the most extreme outlier values. The Yemeni Jews are known not to have a long history at their location (Lourie, 1973). This may be true for the Inuit too, or it could be that they are a special case related to their diet (Jablon- ski and Chaplin, 2000). The next to be removed were two anomalous cells erroneously assigned as inhab- ited by Nunoans that were on the very summit of Andean mountains at extreme UVR; the other cells for Nunoans (on the Altiplano) were left. Lastly, the Bolivians and “mestizos” of Peru were removed, who were both reported to have some mixed blood and whose residuals were large enough to confirm that the admixture was probably great enough to war- rant their removal.

Correlation results

The correlation results were very high when per- formed on the “by cell” data (Table 1). These corre- lations rose as outliers were removed (column 2, Table 1). For the variables containing estimated val- ues derived from either the EEL or the Photovolt readings (column 3, Table 1), all of the correlations between environmental variables and skin reflec- tance measures dropped slightly to about the same level as the raw data in column 1. However, it should be noted that the number of cells rose con- siderably using these data, and this rise probably accounts for much of the small drop in the correla- tions. These measures were then grouped by popu- lation, as explained in Methods, and the correlations for these data are given in the right three columns of Table 1. Most of the variables displayed high collinearity, as would be expected from solar processes or pro- cesses driven by solar energy such as precipitation. There were very high correlations of skin reflectance to UVR, temperature measures, and absolute angle of latitude. UVR Autumn was more highly corre- lated to Melanin (red) Reflectance than was Lati- tude but not for Tissue (blue) Reflectance, where Latitude was more highly correlated. The highest correlation of direct UVR was UVR Autumn, with the absorption peak of Blood (green) Reflectance (r 0.927, d.f. 70, P 0.0001), which was extremely high considering the heterogeneity of the skin color reflectance sample. UVR Autumn, UVR Winter, and UVR Minimum all had r-values greater than the UVR Annual Average for Blood (green) Reflectance and Melanin (red) Reflectance, but not for Tissue (blue) Reflectance, where the UVR Average was highest. It is unlikely that some component of sun- light other than UVR is having an effect, as the variable Total Solar Average Radiation was less cor- related with skin reflectance than was UVR Average or in the UVR Winter and UVR Autumn. The num- ber of days with snow was correlated with lighter colors of skin; another variable with the same pat- tern was Winter Precipitation, which has snow as one of its components.

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G. CHAPLIN

TABLE 1. Pearson correlation coefficients, for skin reflectance measures to environmental variables 1

 

Trimmed by cell for Red Filter

Melanin

Melanin

Tissue

Blood

 

Raw by cell for Red Filter

reflectance by

reflectance

reflectance

reflectance

cell, including

grouped by

grouped by

grouped by

E685.609

E685.609

estimates

population

population

population

d.f. UVR Average UVR Autumn UVR Winter UVR Minimum UVR Spring UVR Summer UVR Maximum UVR Range Latitude Annual precipitation Summer precipitation Winter precipitation Average solar radiation Snow Frost-free days Average temperature, annual Average temperature, summer Average temperature, winter

3,706.0

3,674.0

4,355.0

96.0

70.0

70.0

0.66***

0.69***

0.66***

0.82***

0.89*** 0.86*** 0.86*** 0.82*** 0.79*** 0.78*** 0.79*** ( 0.14)

0.90***

0.76***

0.78***

0.76***

0.84***

0.92***

0.73***

0.75***

0.72***

0.83***

0.93***

0.76***

0.78***

0.76***

0.82***

0.90***

0.18***

0.19***

0.17***

0.65***

0.75***

0.31***

0.33***

0.33***

0.66***

0.73***

0.16***

0.16***

0.16***

0.63***

0.74***

0.54***

0.56***

0.56***

(0.13)

(0.02)

0.75***

0.76***

0.75***

0.83***

0.92***

0.93***

0.16***

0.16***

0.15***

0.23***

0.28***

0.29**

0.05***

0.05**

0.05**

0.32***

0.38***

0.40***

0.26***

0.26***

0.24***

0.35***

0.46***

0.44***

0.27***

0.30***

0.30***

0.63***

0.78***

0.71***

0.35***

0.35***

0.31***

0.46***

0.48***

0.54***

0.36***

0.38***

0.36***

0.59***

0.77***

0.74***

0.42***

0.43***

0.41***

0.67***

0.82***

0.84***

0.09***

0.09***

0.08***

0.38***

0.61***

0.55***

0.55***

0.55***

0.53***

0.71***

0.74***

0.82***

1 Note differences in degrees of freedom of different samples due to differing numbers of missing values. Three left-hand columns show effect, on correlation in data, of having raw data trimmed by having five outliers removed and for data converted from different reflectometers. Three right hand columns are for data summarized by population. All correlations are very highly significant, except UVR Range. * P 0.05. ** P 0.01. *** P 0.0001.

Latitude, UVR Autumn, UVR Winter, UVR Min- imum, and UVR Average were all much more highly correlated to skin reflection measures than were UVR Maximum, UVR Summer, UVR Spring, and all other environmental factors.

Principal components analysis

Principal components analyses were performed on both the trimmed “by cells” and the trimmed “by population” data sets. The results were comparable. The diagnostic metrics for the more significant components, for the grouped “by population” PCA, are given in Table 2. The biplot of this PCA (Fig. 1) represented both the original variables and the transformed observations on the first two principal components axes. The original variables were repre- sented as arrows that graphically indicated the pro- portion of the original variance explained by the first two principal components. The first component comprised the major UVR measures and also was negatively correlated to skin reflectance variables, so that an increase in UVR covaries with a decrease in reflection, which means a darker skin color. The direction of the arrow showed the relative loadings of the variables on PCA components 1 and 2 (S-Plus, 2000). In Figure 1, the arrows span much of the data spread, showing that the two first components accounted for much of the variation (cumulative proportion 0.821). The tem- perature measure arrows were all shorter than

those for other variables, indicating that their co- variance was nested within the variation explained by the UVR measures. The variables UVR Winter (UV Win), UVR Au- tumn (UVAut), UVR Minimum (UV Min), and Win- ter Temperature (Win Tmp) were highly collinear. These four variables showed the greatest negative covariance with skin reflectance measures in the biplot graph (Fig. 1 and Table 2). These four were offset by the number of days with snow on the ground (Snow) and by Winter Precipitation (Winavpcp), which was inclusive of snow. That is, these two variables positively covaried with skin reflectance, with which they grouped. Another group of variables consisted of Total Av- erage Solar Radiation, UVR Maximum, UVR Sum- mer, and Summer Temperature, that lay to the left of the second component axis, and that thereby also correlated with darker skin colors. The variables Frost-Free Days, UVR Average, and Annual Temperature, which were averaging mea- sures of the other variables, lay between the groups from maximum and minimum measures, as would be expected. The loadings showed that most of the variance (65%) was accounted for by the interaction of skin reflectance and snow to solar processes. The next component (17%) showed an axis whereby solar pro- cesses were offset by increasing precipitation, with increases in UVR range being associated with

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297

TABLE 2. Results of principal components analysis by population 1

Importance of components (Comp.)

 

Comp.

Comp.

Comp.

Comp.

 

1

2

3

4

Standard deviation Proportion of variance Cumulative proportion Loadings UVR Summer UVR Autumn UVR Winter UVR Spring UVR Maximum UVR Minimum UVR Range UVR Average Annual average precipitation Summer precipitation Winter precipitation Average solar Average snow days Average frost-free days Average annual temperature Average summer temperature Average winter temperature Tissue (blue) Reflectance Blood (green) Reflectance Melanin (red) Reflectance

 

3.61

1.84

1.08

0.91

0.65

0.17

0.06

0.04

0.65

0.82

0.88

0.92

0.24

 

0.19

0.10

0.26

0.17

0.12

0.26

0.15

0.13

0.25

 

0.19

0.15

0.25

0.20

0.14

0.24

0.21

0.20

 

0.47

0.39

0.27

0.45

0.45

0.39

0.44

0.15

0.22

0.32

0.44

0.25

0.21

 

0.18

0.34

0.63

0.25

 

0.24

0.26

0.23

0.21

 

0.22

0.23

0.22

0.24

0.17

0.16

0.29

 

0.26

0.11

0.20

0.26

0.14

0.20

0.24

0.16

0.25

1 Number of variables is 20; number of observations is 69.

lighter skin reflectance in the longer wavelength reflectance but not for Tissue (blue) Reflectance. Tis- sue (blue) Reflectance was negatively correlated (darker skin reflectance) on the minor third axis (6%) with snow and harsh winter weather. The last axis, which was below 5%, was the contrast between snow days and other Winter Precipitation, where a decrease in snow and an increase in other forms of winter precipitation were correlated with a lighter skin reflectance.

Regression analysis

It was possible to use the correlations (Table 1) and the PCA analysis (Table 2) to pick variables warranting greater investigation (Johnston, 1978). UVR Autumn appeared to be the main single effec- tor, and UVR Maximum with Summer Precipitation were very minor effectors. These were offset by pre- cipitation in the winter (which includes, in part, the number of days with snow). The PCA showed that the temperature measures appeared to be so closely aligned to the UVR values that they could be ignored. This was confirmed by performing regressions with nested variables. For example, Blood (green) Reflectance alone to UVR Autumn had a higher coefficient of determination than that for Blood (green) Reflectance and Average Temperature together or Average Temperature alone. The contribution of Average Temperature was also nonsignificant (P 0.25, d.f. 69). This is not to say that variation in temperature measures lacked explanatory power, but rather they were so collinear with UVR that they had no extra indepen-

were so collinear with UVR that they had no extra indepen- Fig. 1. Biplot of component

Fig. 1. Biplot of component 1 vs. component 2 of PCA of skin reflectance measures and environmental variables of grouped “by population” data. Melanin (red), Blood (green), and Tissue (blue) Reflectances are tightly grouped to right on first axis, and loosely grouped with average snow days (Snow) and Winter Precipitation (Winpcp). All other variables are on opposite side of central axis. Directly opposite to skin reflectance variables is a cluster of UVR Winter (UV Win), UVR Autumn (UV Aut), UVR Minimum (UV Min), and Average Winter Temperature (Wintmp). UVR Range (UV Range) with Summer Precipitation (Sumpcp) and Annual Precipitation (Anpcp) are on an orthogonal axis. AvRad, average solar radiation; UvMax, UVR maximum; Sumtp, summer tem- perature; UvSum, UVR summer; UvSprg, UVR Spring; Ffree, no. of frost-free days; UvAvg, UVR average; Avtmp, average temper- ature.

dent explanatory power over that of UVR; therefore, they were omitted. The weak relationship of Summer Precipitation to skin reflectance measures was highly significant (r 2 0.403, d.f. 70, P 0.0001). Correlation, PCA, and stepwise regression vali- dated the four-variable linear model developed. The results are given in Table 3. All r 2 values were impressively high (multiple r 2 :

Melanin (red) Reflectance 0.7283, Tissue (blue) Reflectance 0.8327, and Blood (green) Reflec- tance 0.8872; the nonsignificant coefficient (Win- ter Precipitation) added, at most, 0.017 to the r 2 value). There was a greater spread in the fitted values than in the residuals; the quartile-quartile fit of the residuals was not significantly different from normal; and there were very few outliers. These observations further validate the competency of the linear model. In conclusion, the multiple-regression model was an adequate straight-line approximation of the relationship between variables.

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G. CHAPLIN

 

TABLE 3. Table of diagnostic statistics of multiple regression equations

  TABLE 3. Table of diagnostic statistics of multiple regression equations

Blue Tissue Reflectance UVR Autumn UVR Maximum Summer Precipitation Winter Precipitation

 

Standard

Coefficients

Value

error

t-value

P

Intercept

41.7231

2.4860

16.7834

0.0001

UVAUT 0.0457 UVMAX 0.0365 SUMAVPCP 0.0014

0.0080

5.7156

0.0001

0.0072

5.0912

0.0001

0.0004

3.2372

0.0019

WINAVPCP 0.0006 0.0011

0.5947

0.5540

Residual standard error: 4.396 on 67 degrees of freedom Multiple r 2 : 0.8327 F-statistic: 83.39 on 4 and 67 degrees of freedom, P 0.0001 Outliers: Japan Hidakka, Eastern Nepal

Green Blood Reflectance UVR Autumn UVR Maximum Summer Precipitation Winter Precipitation

 

Standard

Coefficients

Value

error

t-value

P

Fig. 2. Spline graph of relationship of green filter reflectance, which approximates that of blood absorption, to UVR Maximum (UVMAX).

Intercept

43.5006

2.2443

19.3825

0.0001

UVAUT 0.0758

0.0071

10.7087

0.0001

UVMAX 0.0156 0.0065

2.4072

0.0188

SUMAVPCP 0.0011

0.0004

2.9080

0.0049

WINAVPCP 0.0018 0.0009

1.8976

0.0621

showed a few interesting findings. UVR Autumn had a linear relationship with skin reflectance, whereas UVR Maximum’s straight-line relationship only extended up to the limit of that for UVR Au- tumn, above which the relationship failed. The dis- tribution of populations in areas beyond this level of UVMED showed a high level of variance. There was a suggestion of a much lower correlation of UVR Maximum to darker skin color above this value (Fig. 2). Precipitation in the summer seemed to follow the pattern of UVR Maximum to which it was uncorre-

Residual standard error: 3.977 on 67 degrees of freedom Multiple r 2 : 0.8872 F-statistic: 131.7 on 4 and 67 degrees of freedom, p 0.0001 Outliers: Eastern Nepal, Yemen

Red Melanin Reflectance UVR Autumn UVR Maximum Summer Precipitation Winter Precipitation

 

Standard

Coefficients

Value

error

t-value

P

Intercept

63.0801

3.8472

16.3963

0.0001

UVAUT 0.1014

0.0114

8.9182

0.0001

UVMAX

0.0035

0.0111

0.3186

0.7507

SUMAVPCP 0.0001

0.0006

0.2310

0.8178

WINAVPCP 0.0028 0.0014

1.9205

0.0579

Residual standard error: 7.342 on 92 degrees of freedom Multiple r 2 : 0.7283 F-statistic: 61.66 on 4 and 92 degrees of freedom, P 0.0001 Outliers: Australia Darwin, Cambodia, Namibia, and Yemen

lated (r 0.044, P 0.67). Winter precipitation had a weak opposite effect.

Categorical variables for forest and relief

 

Spatial bias and autoregression

The analysis of variance produced nonsignificant results and will not be reported. The boxplots of the data (not shown) indicated why these nonsignificant results were obtained. All variables had ranges that overlapped, except for UVR Maximum, in high and middle mountains, and Melanin (red) Reflectance, where there does appear to be a small nonsignificant influence of topographic relief on skin reflectance.

Mapping environmental data

The correlation of the regression residuals with either absolute angle of latitude or longitude or both was zero, showing that there was an absence of spatial bias in the residuals. The residuals were normally distributed, and there was a very close concordance of the model to the data. The residuals of the multiple regression against both latitude and longitude showed that there was no unaccounted-for variation related to geography, i.e., latitude, longi- tude, or the latitude:longitude interaction. The test for hemispheric differences did not find a noticeable difference in pattern, contra Relethford (1997). There was a slight nonsignificant difference in magnitude of response (as found by Relethford, 1997), which was considered the result of sampling. Therefore, it is safe to assume that modern humans are one population for statistical purposes.

Nonlinear graphing

The map of UVR Autumn was very similar to that for Annual Average UVR (Jablonski and Chaplin, 2000). The predominant effect caused by the angle of the sun to the ozone layer manifested itself as lati- tudinal bands of nearly equal UVR. Over the land, these bands were modified by factors related to wa- ter vapor, monsoon effects related to the size of the west-to-east extent of the land masses, and altitude. Autumn was without extremes of UVR. In autumn, there is a monsoon “continental effect,” i.e., an ame- lioration of UVR on the eastern side of land masses. The effects of climate are more stable in autumn- winter than in summer, which brings monsoons and summer rain, and droughts around the tropics. Spring had higher levels of UVR than autumn due to

Nonlinear methods do not provide good diagnostic statistics. The nonlinear individual variable graphs

ENVIRONMENT AND HUMAN SKIN COLORATION

299

ENVIRONMENT AND HUMAN SKIN COLORATION 299 Fig. 3. Map of skin color reflectance predicted from multiple

Fig. 3.

Map of skin color reflectance predicted from multiple regression. Map is generalized to reduce number of polygons.

drying prior to the monsoon. The lowest mean and coefficient of variation were in autumn. The map for UVR Range showed some unexpected results. The range was lowest in the large equatorial rainforest areas. There the range was about the same as in Greenland, where the range was com- pressed by the low potential maximum. Northern Europe had higher ranges than equatorial regions, and the Mediterranean area was considerably higher. The highest values for range were in the high-altitude deserts, which also have the highest UVR values. Snow followed latitude to a great degree except for Tibet, the southern Andes, Iran, Turkey, the Trans- Caucasus, and Japan. The pattern discernible in autumn UVR had higher values in Africa than in other equatorial re- gions. Africa was the most heterogeneous continent with respect to UVR regimes, due to its large latitu- dinal range, large west-to-east extent north of the equator, a wide variety of humidity regimes, and a large altitudinal range from west to east (and within the east from north to south).

Map of skin color reflectance predicted from multiple regression formulae

The map of predicted skin colors produced from the multiple regression formulae had more than 26,000 features, and the legend had over 1,200 unique combinations of the three reflectance values. The maps of predicted values showed that skin color reflectance was predicted to be more heterogeneous in Africa. There were similar small niches in all areas of high UVR near the equator. Areas with the lowest value for predicted skin color reflectance were in New Zealand’s South Island fjords, Greenland, and Tierra del Fuego. The next lowest predictions were areas in Scandinavia and the northwestern

British Isles. The area with the darkest predicted values for skin reflectance were on the mountain peaks of the Andes and the Ethiopian highlands. It was easy to see in these maps that skin reflectance would be predicted to be a fairly smooth gradation of values with disjuncts only at the most major of geo- morphologic barriers such as the Himalayas. In ar- eas away from the Equator, the size of ecological patches increases with increasing latitude. This ef- fect was mostly lost in the Southern Hemisphere due to the lack of land farther to the south at high latitudes. At smaller scales, the colors almost com- pletely blend into one another, making the clinal nature of skin color obvious. Therefore, the general- ized map is of more use for visualizing the data.

DISCUSSION

The first and more popular hypothesis to be tested (that reduced skin reflectance is related to direct exposure to UVR) is only weakly supported by this study. There are lower correlations, and a much smaller contribution in the regression analysis, for measures of periods of high UVR, e.g., skin reflec- tance and UVR Maximum, UVR Summer, and UVR Spring. These measures explain at least 17% less of the variation in the data than those for times of low UVR. This observation argues strongly against sun- burning or sun-induced cancer as major causative agents in the evolution of skin coloration, because these diseases are modulated by UVB (summer UVR). This result was predicted because cancers arise mostly after the human reproductive career has ended (Blum, 1961; Jablonski and Chaplin,

2000).

The breakdown of the linear response of skin re- flectance to UVR Maximum at very high levels of UVR, as seen in the nonlinear techniques, indicates that these populations exhibited a large range of

300

G. CHAPLIN

values and much variation about the line. The dark- est people seemed to be those who have inhabited their homelands for very long periods of time, e.g., Australian Aborigines and Ethiopians. As these pop- ulations are those that seem to be resident the long- est, it can be concluded that the final increments of skin darkening appear to have required longer to evolve. The darkest populations have similar reflec- tance values, so that there may be a point where it is not biologically possible to darken further, and ap- proaching that point will slow the rate of adaptation. The prediction that there is reduced skin reflec- tance in the Tissue (blue) Reflectance range due to thickening of the stratum corneum caused by UVR is supported. Tissue (blue) Reflectance was slightly more correlated with UVR Maximum than were the other reflectance measures, a finding that helps to explain the thickened stratum corneum found in African populations, although a thickened stratum corneum would provide little photo-protection, as can be seen in people with pigment disorders (Rob- ins, 1991). The second set of hypotheses, concerning theories of metabolic processes relating direct solar radiation to skin reflectance, finds the strongest support. The main original finding of this study was that the evolution of skin color reflectance could be almost fully modeled as a linear effect of UVR in the au- tumn alone (UVR Autumn with the absorption peak of Blood (green) Reflectance; r 0.927, d.f. 70, P 0.0001). This is also true for all measures of the period of lower UVR (those with an increased pro- portion of longer-wavelength UVR): UVR Autumn, UVR Minimum, and UVR Winter. These measures were all more important at explaining skin reflec- tance variation than were the peak UVR measures. This very strong finding gives considerable support to the nutrient hypothesis. Folate photolysis leading to folate deficiency was proposed as an agent de- creasing fitness and promoting skin darkening in lower latitudes near the Equator out to beyond the tropics (Jablonski, 1992, 1999; Jablonski and Chap- lin, 2000). Hypovitaminosis D was found to be the agent in higher latitudes where there are prolonged periods without vitamin-D-promoting UVR (UVB) (Holick, 1995; Jablonski and Chaplin, 2000; Loomis, 1967). High levels of wintertime UVA without UVB, as found in middle latitudes, would destroy both vitamin D and folate by photolysis. This extremely well-fitted linear model explains why latitude was such a good surrogate for UVR, because Latitude and UVR Autumn were extremely highly correlated (r 0.967, d.f. 102, P 0.0001), as was Latitude and UVR Average (r 0. 937, d.f. 102, P 0.0001), but not Latitude and UVR Sum- mer (r 0.767, d.f. 102, P 0.0001). Further, this indicates that latitude is still useful for human eco- logical modeling. Hypotheses about variables that are only corre- lated to UVR by latitude or through solar-driven processes such as vegetation, temperature, and pre-

cipitation generally received little support, although these variables may alter the response of skin to UVR and so magnify or mitigate the other two groups of hypotheses. The inability of any of the temperature measures to explain variation in the regression analysis indi- cated that the small differences in thermoregulatory performance of different skin colors seemed to be swamped by the nutrient requirements and protec- tive roles of skin. Frost and Winter Precipitation in the PCA and regression results provide tenuous support to the structural reduction hypothesis by Brace (1963), where defects accumulate in the pigmentary system in the absence of positive selection. However, the cultural adaptations of shelter-seeking and clothes- wearing would have exaggerated problems with hy- povitaminosis D. This was documented for immi- grants into Northern Europe (Henderson et al., 1987; Hodgkin et al., 1973; Solanki et al., 1995). The last two factor loadings of the PCA indicate that there was a contrast in the effects of precipita- tion measures. Tissue (blue) Reflectance was nega- tively correlated on the minor third axis (6%) with harsher winter weather, i.e., harsh weather was correlated with darker skin in the blue spectrum. This could be because of the response to extremes of climate that cause trauma that thickens the stra- tum corneum. This effect may be magnified by higher altitude. This mechanism could also account for some of the different correlation observed for Tissue (blue) Reflectance in the correlation and re- gression analysis compared to the other skin reflect- ences. All the analysis methods show that Summer Pre- cipitation is correlated with darker skin color. This effect is nonlinear and mirrors that seen in the re- sponse to UVR Maximum. It appears to magnify the effect of UVR. This finding adds support to Gloger’s rule. Summer rain, particularly in warmer regions, promotes sweating, which causes blood to rise into the dermis to supply the sweat glands. Under these conditions, the blood and its nutrients will be more susceptible to UVR damage. In addition, wet skin allows the skin to become more transparent to UVR by refraction, so that sweating effectively lowers the minimal erythemal dose (Moehrle et al., 2000). The maps of predicted values of skin coloration were consistent with findings by Relethford (2000) that skin reflectance was more variable in Africa, and that in areas where the size of ecological patches is larger with increased latitude (primarily Eur- asia), there was less diversity in skin color. This is a result explained here by diversity and size of climate niches. The four-term multiple regression was very successful and was able to model complex relation- ships across relatively small areas, such as Micro- nesia, which showed a great diversity of habitats within an area of limited latitudinal range. This study confirms the observation that skin col- oration is adaptive and clinal in nature, although

ENVIRONMENT AND HUMAN SKIN COLORATION

301

the adaptation of skin color to Summer UVR seemed to reach a threshold beyond which further adapta- tion through increasing melanization was difficult. The conclusion of an adaptive cline was supported by: 1) the very high level of correlation between skin reflectance and environmental variables; 2) a nearly straight-line fit of skin reflectance to UVR Autumn, which was highly suggestive of a one-to-one re- sponse; and 3) the very low number of variables that were able to account for the majority of variation in the data. Although this does not constitute proof of a causal relationship between skin reflectance and en- vironmental factors, this combination of factors greatly increases the likelihood that one exists. This is a position that was supported for other geograph- ically varying associations, e.g., disease (Foster,

1987).

ACKNOWLEDGMENTS

The author thanks Elizabeth Weatherhead for providing access to the NASA TOMS UVMED data, to Kenneth Beals for providing a digital copy of the unpublished database collated at Oregon State Uni- versity, and to Charles Convis of the Environmental Systems Research Institute (ESRI) for donations of GIS software and data. The author thanks C. Philip Wheater and Tom Poiker for their timely help and advice. The author also thanks Nina G. Jablonski for advice and fruitful discussions.

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APPENDIX I. Skin reflective values used in this study.

Reflectance

Name

Ref.

Tissue

Blood

Melanin

How mapped

Various Huachipaeri Mexico Shipibo Slovakia United Kingdom United Kingdom & Northern Ireland United States, Florida United States, Oklahoma United States, Western

1

Various Estimated from atlas Estimated as sierra region Estimated from atlas Western region of Slovakia Estimated from atlas Estimated from atlas Estimated from atlas Estimated from atlas Estimated from atlas

2

12.8

19.1

48.6

2

19.3

27.1

48.1

2

15.75

21.4

53.2

3

28.8

36.9

62.5

4

42.3

45.6

69

4

42.3

45.6

68.9

5

47.7

5

50.4

6

19.1

33.3

1 References (Ref.) for data: 1, Jablonski and Chaplin, 2000; 2, Ebbinghaus, 1966; 3, Sefcakova, 1986; 4, Little and Wolff, 1981; 5, Pollitzer et al., 1970; 6, Pawson and Petrakis, 1975. Full references in Chaplin (2001).