Genetic evidence and the modern human origins debate.

A continued debate in anthropology concerns the evolutionary origin of 'anatomically modern humans' (Homo sapiens sapiens). Different models have been proposed to examine the related questions of (1) where and when anatomically modern humans first appeared and (2) the genetic and evolutionary relationship between modern humans and earlier human populations. Genetic data have been increasingly used to address these questions. Genetic data on living human populations have been used to reconstruct the evolutionary history of the human species by considering how global patterns of human variation could be produced given different evolutionary scenarios. Of particular interest are gene trees that reconstruct the time and place of the most recent common ancestor of humanity for a given haplotype and the analysis of regional differences in genetic diversity. Ancient DNA has also allowed a direct assessment of genetic variation in European Neandertals. Together with the fossil record, genetic data provide insight into the origin of modern humans. The evidence points to an African origin of modern humans dating back to 200,000 years followed by later expansions of moderns out of Africa across the Old World. What is less clear is what happened when these early modern humans met preexisting 'archaic human' populations outside of Africa. At present, it is difficult to distinguish between a model of total genetic replacement and a model that includes some degree of genetic mixture.

Absence of regional affinities of Neandertal DNA with living humans does not reject multiregional evolution.

The recent extraction of mitochondrial DNA sequences from three European Neandertal fossils has led many to the conclusion that ancient DNA analysis supports the African replacement model of modern human origins and rejects models of multiregional evolution that propose some Neandertal ancestry in living humans. This conclusion is based, in part, on the lack of regional affinity of Neandertal DNA to that from living Europeans. Consideration of migration matrix models shows that this conclusion is premature, since under a model of interregional gene flow we expect to see similar levels of Neandertal ancestry in all contemporary regions, and living Europeans should not necessarily show closer affinity. The absence of regional affinity in Neandertal DNA does not distinguish between replacement and multiregional models.

Global analysis of regional differences in craniometric diversity and population substructure.

Estimates of genetic diversity in major geographic regions are frequently made by pooling all individuals into regional aggregates. This method can potentially bias results if there are differences in population substructure within regions, since increased variation among local populations could inflate regional diversity. A preferred method of estimating regional diversity is to compute the mean diversity within local populations. Both methods are applied to a global sample of craniometric data consisting of 57 measurements taken on 1734 crania from 18 local populations in six geographic regions: sub-Saharan Africa, Europe, East Asia, Australasia, Polynesia, and the Americas. Each region is represented by three local populations. Both methods for estimating regional diversity show sub-Saharan Africa to have the highest levels of phenotypic variation, consistent with many genetic studies. Polynesia and the Americas both show high levels of regional diversity when regional aggregates are used, but the lowest mean local population diversity. Regional estimates of F(ST) made using quantitative genetic methods show that both Polynesia and the Americas also have the highest levels of differentiation among local populations, which inflates regional diversity. Regional differences in F(ST) are directly related to the geographic dispersion of samples within each region; higher F(ST) values occur when the local populations are geographically dispersed. These results show that geographic sampling can affect results, and suggest caution in making inferences regarding regional diversity when population substructure is ignored.

Human skin color diversity is highest in sub-Saharan African populations.

Previous studies of genetic and craniometric traits have found higher levels of within-population diversity in sub-Saharan Africa compared to other geographic regions. This study examines regional differences in within-population diversity of human skin color. Published data on skin reflectance were collected for 98 male samples from eight geographic regions: sub-Saharan Africa, North Africa, Europe, West Asia, Southwest Asia, South Asia, Australasia, and the New World. Regional differences in local within-population diversity were examined using two measures of variability: the sample variance and the sample coefficient of variation. For both measures, the average level of within-population diversity is higher in sub-Saharan Africa than in other geographic regions. This difference persists even after adjusting for a correlation between within-population diversity and distance from the equator. Though affected by natural selection, skin color variation shows the same pattern of higher African diversity as found with other traits.

Spatial variation of anthropometric traits in Ireland.

To further elucidate the relationship between geography and genetics in Ireland, we considered variation in anthropometric traits of adult males by town using spatial autocorrelation methods. By describing and distinguishing significant patterns of anthropometric variation, we determined whether the anthropometric traits display a simple pattern of spatial variation, as predicted by the isolation by distance model, or other patterns of spatial variation. Several hypotheses were examined, including (1) whether there was spatial patterning of 20 anthropometric phenotypic distributions and 7 principal components of Irish males and (2) if there was, whether these phenotypic distributions could be explained by a simple isolation by distance model. The results of this study can be summarized by several key findings: (1) There is significant spatial patterning among towns, as detected in correlograms of 14 anthropometric traits and 2 principal component factor scores (values of Moran's I ranging from 0.7510 to -0.3616, p < or = 0.0071); (2) 4 spatial patterns were detected, including clinical patterns, long-distance differentiation, distance distinction, and regional patchiness. These results suggest several likely causes of the observed spatial patterns. First, in Ireland patterns of anthropometric variation could not be explained by a single spatial pattern (i.e., isolation by distance). Second, through an examination of the various combinations of statistical homogeneity or heterogeneity, spatial patterning or nonpatterning, and similarity or dissimilarity of spatial patterns, we conclude that several migrational events structured the genetic landscape of Ireland.

Genetic evidence for larger African population size during recent human evolution.

Genetic evidence suggests that the long-term average effective size of sub-Saharan Africa is larger than other geographic regions. A method is described that allows estimation of relative long-term regional population sizes. This method is applied to 60 microsatellite DNA loci from a sample of 72 sub-Saharan Africans, 63 East Asians, and 120 Europeans. Average heterozygosity is significantly higher in the sub-Saharan African sample. Expected heterozygosity was computed for each region and locus using a population genetic model based on the null hypothesis of equal long-term population sizes. Average residual heterozygosity is significantly higher in the sub-Saharan African sample, indicating that African population size was larger than other regions during recent human evolution. The best fit of the model is with relative population weights of 0.73 for sub-Saharan Africa, 0.09 for East Asia, and 0.18 for Europe. These results are similar to those obtained using craniometric variation for these three geographic regions. These results, combined with inferences from other genetic studies, support a major role of Africa in the origin of modern humans. It is less clear, however, whether complete African replacement is the most appropriate model. An alternative is an African origin with non-African gene flow. While Africa is an important region in recent human evolution, it is not clear whether the gene pool of our species is completely out of Africa or predominately out of Africa.

Mitochondrial DNA and ancient population growth.

In recent years, the study of mitochondrial DNA (mtDNA) variation has entered a new phase with an increasing emphasis on interpretations of demographic, rather than phylogenetic, history. Human mtDNA variation fits a "sudden expansion" model, where the human species expanded rapidly in size during the Late Pleistocene. This paper examines the sudden expansion model with the goal of partitioning total mtDNA diversity in contemporary populations into two components--diversity that existed prior to the population expansion and diversity that arose after the expansion. A method is developed for estimating these components. Analysis of mtDNA diversity within selected human populations shows that 64-80% of mtDNA diversity in contemporary populations arose after the expansion, a consequence of a high mutation rate relative to the number of generations since expansion. The basic model is extended to two components of excess diversity in sub-Saharan Africa--differences in population size before the expansion and differences in the timing of expansion. Results suggest that excess sub-Saharan African mtDNA diversity is due to the combined effects of the sub-Saharan African population being larger in size prior to the expansion and expanding earlier.

Influence of religion and birthplace on the genetic structure of Northern Ireland.

The effect of geographic and religious subdivision on the genetic structure of Northern Ireland was assessed using data on 10 craniofacial measurements collected on 755 adult males that were born in five counties and belonged to one of three religious affiliations (Catholic, Church of Ireland, Presbyterian). Fifteen samples were defined based on birth county and religious affiliation. Two-way univariate and multivariate analysis of variance shows significant effects of birth county and religious affiliation, with somewhat greater subdivision due to religion. Distance matrix correlations reveal a small, but significant, effect of birth county and religious affiliation on the pattern of genetic distances between the 15 samples, with a slightly greater influence of religion. The Church of Ireland samples show the greatest differences. perhaps revealing the combined influence of differential population origins and religious differences as a barrier to gene flow. Overall, religion has a significant, though minor, influence on genetic variation in Northern Ireland.

Mutation rate and excess African heterozygosity.

Global studies of within-group genetic variation have revealed a tendency for some traits, but not all, to show higher heterozygosity in sub-Saharan African populations. Although excess African diversity has been interpreted as reflecting a greater "age" of sub-Saharan African populations, more recent research has shown that this excess is more likely a consequence of a larger African long-term effective population size. The observation that certain traits, particularly classic genetic markers and RFLPs, do not show this pattern has been interpreted as ascertainment bias. Here, I examine another possible factor: that excess African heterozygosity is in part a function of mutation rate. Simple equilibrium and nonequilibrium models of absolute excess heterozygosity are examined. The results indicate that there is little excess African heterozygosity for traits with low mutation rates and greater excess heterozygosity for traits with moderate to high aggregate mutation rates. Observed data are consistent with these models. Also, depending on population size and time depth, traits with high levels of mutation might show less excess heterozygosity than those with moderate to high mutation rates. Another measure of diversity, mean sequence divergence, shows an increase in excess diversity for traits with high mutation rates.

Genetic drift and gene flow in post-famine Ireland.

This study examines the genetic impact of the Great Famine (1846-1851) on the regional genetic structure of Ireland. The Great Famine resulted in a rapid decrease in population size throughout Ireland in a short period of time, increasing the possibility of genetic drift. Our study is based on migration and anthropometric data collected originally in the 1930s from 7211 adult Irish males. These data were subdivided into three time periods defined by year of birth: 1861-1880, 1881-1900, and 1901-1920. Within each time period the data were further subdivided into six geographic regions of Ireland. Estimates of Wright's FST were calculated from parent-offspring migration data and from 17 anthropometric variables (10 head measures, 7 body measures). Over time, the average population size decreased, but average rates of migration increased. The estimates of FST at equilibrium from migration matrix analysis suggest that the net effect of these opposite effects is a reduction in among-group variation. Closer examination shows that within each time period the rate of convergence to equilibrium is slow, meaning that the expected levels of genetic homogeneity revealed from migration matrix analysis are not likely to be seen over short intervals of time. Estimates of FST from anthropometric data show either relatively little change in microdifferentiation or some increase, depending on which variables are analyzed. Investigation of a simple model of demographic and genetic change shows that, given the demographic changes in post-Famine Ireland, FST could in theory increase, decrease, or remain the same over short intervals of time. Overall, the Great Famine appears to have had minimal impact on the genetic structure of Ireland on a regional level. Comparison with studies focusing on local genetic structure shows the opposite. It appears that the level of genetic impact depends strongly on the level of analysis; local populations are affected to a greater extent by demographic shifts than regional populations. We also provide formulas for the standard errors of FST from metric traits and related statistics.

Hemispheric difference in human skin color.

Previous studies of human skin color have shown a strong relationship between skin color and distance from the equator, which has been interpreted as a link between skin color, latitude, and the intensity of ultraviolet radiation. The underlying assumptions are that UV radiation is greatest at the equator and that it diminishes with increasing latitude to the same extent in both the Northern and Southern Hemispheres. The standard analysis of human skin color is based on these assumptions, such that skin color is assumed to be darkest at the equator, and the decrease of skin color with latitude is assumed to be the same in both hemispheres. A nonlinear piecewise regression model was developed to test these assumptions and applied to mean skin reflectance data from 102 male samples and 65 female samples from across the Old World. For both males and females, skin reflectance (%) is lowest at the equator (darkest skin). Among males, skin reflectance increases roughly 8.2% for every 10 degrees of latitude in the Northern Hemisphere but only 3.3% for every 10 degrees of latitude in the Southern Hemisphere. Among females, the corresponding numbers are 8.1% in the Northern Hemisphere and 4.7% in the Southern Hemisphere. These results indicate that human skin color is darker in the Southern Hemisphere than in the Northern Hemisphere at equivalent latitude. Recent research shows that UV radiation is higher in the Southern Hemisphere than in the Northern Hemisphere at similar latitude. This difference, relating to astronomical and climatic conditions, may have existed in the past at different times and perhaps influenced the evolution of human skin color.

Genetic drift can obscure population history: problem and solution.

Genetic distances between populations can be derived from a wide variety of data and have been applied to studies of population structure and history ranging from local groups to an entire species. Genetic distances measure the effects of both population history (historical relations and migration) and population structure (migration and drift). Frequently, we are interested in assessing population history, and any impact of differential genetic drift is likely to confound our interpretations. I show here that when population sizes are different, differential genetic drift can obscure the underlying pattern of population history. Previous genetic distance studies have failed to take genetic drift into account when reconstructing population history. A simple method is presented here that takes into account differences in population size and differential drift. This method is illustrated using allele frequencies from Jewish and non-Jewish populations in six Old World regions. The scaled distances provide a clearer picture of population history than the traditional unscaled distances.

Anthropometric variation and the population history of Ireland.

Genetic variation among human populations can reflect a combination of contemporary patterns of gene flow and genetic drift as well as long-term population relationships due to population history. We examine the likely impact of past history and contemporary structure on the patterns of anthropometric variation among 31 counties in Ireland (made up of the two nations of the Republic of Ireland and Northern Ireland). Data for 17 anthropometric measures and parent-offspring migration on 7,214 adult Irish males were taken from the large data set originally collected by Dupertuis and Dawson in the mid-1930s (Hooton et al., 1955). Patterns of genetic similarity among 31 counties were assessed using R matrix methods that allow estimation of minimum genetic distances. These distances were compared to distances reflecting history, geography, and migration using matrix permutation methods. The results indicate that among-group variation in Ireland reflects past population history to a much greater extent than contemporary patterns of migration and population size. The midland counties are distinct from other populations, and their history suggests greater genetic input from early Viking invasions. A second major pattern in biological variation is a longitudinal gradient separating western and eastern counties. This gradient appears related to patterns of early settlement and/or a concentration in the east of later immigrants, particularly from England. Comparison of regional means with published data for several other European nations confirms these hypotheses.

Craniometric variation, genetic theory, and modern human origins.

Recent controversies surrounding models of modern human origins have focused on among-group variation, particularly the reconstruction of phylogenetic trees from mitochondrial DNA (mtDNA) and the dating of population divergence. Problems in tree estimation have been seen as weakening the case for a replacement model and favoring a multiregional evolution model. There has been less discussion of patterns of within-group variation, although the mtDNA evidence has consistently shown the greatest diversity within African populations. Problems of interpretation abound given the numerous factors that can influence within-group variation, including the possibility of earlier divergence, differences in population size, patterns of population expansion, and variation in migration rates. We present a model of within-group phenotypic variation and apply it to a large set of craniometric data representing major Old World geographic regions (57 measurements for 1,159 cases in four regions: Europe, Sub-Saharan Africa, Australasia, and the Far East). The model predicts a linear relationship between variation within populations (the average within-group variance) and variation between populations (the genetic distance of populations to pooled phenotypic means). On a global level this relationship should hold if the long-term effective population sizes of each region are correctly specified. Other potential effects on within-group variation are accounted for by the model. Comparison of observed and expected variances under the assumption of equal effective sizes for four regions indicates significantly greater within-group variation in Africa and significantly less within-group variation in Europe. These results suggest that the long-term effective population size was greatest in Africa. Closer examination of the model suggests that the long-term African effective size was roughly three times that of any other geographic region. Using these estimates of relative population size, we present a method for analyzing ancient population structure, which provides estimates of ancient migration. This method allows us to reconstruct migration history between geographic regions after adjustment for the effect of genetic drift on interpopulational distances. Our results show a clear isolation of Africa from other regions. We then present a method that allows direct estimation of the ancient migration matrix, thus providing us with information on the actual extent of interregional migration. These methods also provide estimates of time frames necessary to reach genetic equilibrium. The ultimate goal is extracting as much information from present-day patterns of human variation relevant to issues of human origins.(ABSTRACT TRUNCATED AT 400 WORDS)

Craniometric variation among modern human populations.

Previous studies of genetic markers and mitochondrial DNA have found that the amount of variation among major geographic groupings of Homo sapiens is relatively low, accounting for roughly 10% of total variation. This conclusion has had implications for the study of human variation and consideration of alternative models for the origin of modern humans. By contrast, it has often been assumed that the level of among-group variation for morphological traits is much higher. This study examines the level of among-group variation based on craniometric data from a large sample of modern humans originally collected by W. W. Howells. A multivariate method based on quantitative genetics theory was used to provide an estimate of FST--a measure of among-group variation that can be compared with results from studies of genetic markers. Data for 57 craniometric variables on 1,734 crania were analyzed. These data represent six core areas: Europe, Sub-Saharan Africa, Australasia, Polynesia, the Americas, and the Far East. An additional set of analyses was performed using a three-region subset (Europe, Sub-Saharan Africa, and the Far East) to provide comparability with several genetic studies. The minimum FST (assuming complete heritability) for the three-region analysis is 0.065, and the minimum FST for the six-region analysis is 0.085. Both of these are less than the average FST from genetic studies (average estimates of 0.10-0.11). The smaller value of the minimum FST estimates is expected since it provides an estimate of FST expected under complete heritability. Using an estimate of average craniometric heritability from the literature provides an estimate of FST of 0.112 for the three-region analysis and 0.144 for the six-region analysis. These results show that genetic and craniometric data are in agreement, qualitatively and quantitatively, and that there is limited variation in modern humans among major geographic regions.

Temporal trends in migration in the Aland Islands: effects of population size and geographic distance.

Using a model developed by Relethford (1992), we assess temporal trends (1750-1949) in marital migration in the Aland Islands, Finland, in relation to both geographic distance and population size. The 200-year time period was divided into four 50-year periods. For all time periods both geographic distance and population size are important determinants of migration among 15 Lutheran parishes. The geographic distance parameter of the model decreases significantly over time, and the population size parameter fluctuates slightly but shows no significant change over time. For all time periods migration is negative density dependent, indicating that there is greater relative flow from larger to smaller subdivisions. Even though both the geographic distance and population size parameters are statistically significant, the analysis suggests that geographic distance has a greater relative effect on migration than population size. There is a clear indication of isolate breakdown during the last two time periods (1850-1899 and 1900-1949). Residual analysis indicated that the smallest parish (Sottunga) was a major outlier that showed greater exogamy (less endemicity) than expected from the model.

Marital exogamy in the Aland Islands, Finland, 1750-1949.

Marriage records from 1750 through 1949 were used to examine effects of population size, geographic distance, and temporal change on rates of marital exogamy in the Aland Islands, Finland. Exogamy rates for individuals (not couples) were computed for 15 Aland parishes in each of four 50-year time periods, giving a total of 60 observations. These rates were analysed with respect to population size using a quadratic regression model. Regression analyses were also used to examine the relationship of marital exogamy with two measures of geographic distance--average distance to all other parishes and nearest-neighbour distance. Analysis of variance was used to examine temporal trends. Multiple regression analyses were used to examine all of these factors simultaneously. Marital exogamy is highest in smaller and larger populations, and less in medium-sized populations. Higher exogamy rates in small populations are related to the lack of available mates in small groups. Higher exogamy rates in larger populations may reflect economic attraction of larger groups. Exogamy rates are lower in the more geographically isolated parishes. From 1750 through 1899 there is little change in exogamy rates, whereas exogamy rates double after 1900. This temporal change reflects changes in transportation technology and other cultural factors promoting increased migration. The multiple regression model shows population size, geographic distance, and temporal change are all significant correlates of exogamy, collectively explaining a large percentage of variation in rates (R2 = 0.79).

Cross-cultural analysis of migration rates: effects of geographic distance and population size.

A model is developed that treats migration rates among populations as a function of the geographic distance between them and the size of both sources and recipient population. Specifically, mij/mjj = a(Ni/Nj)pe-bd, where mij/mjj is the relative migration rate into population j from population i, Ni is the size of the source population, Nj is the size of the recipient population, d is the geographic distance between populations i and j, p is a measure of differential density-dependence, b is a measure of distance decay, and a is an adjustment parameter with little demographic meaning. Methods of parameter estimation and hypothesis testing using maximum likelihood are outlined. These methods are applied to migration matrix data from 13 samples obtained from the literature representing a wide range of ecological settings. All samples show a significant effect of geographic distance on migration, and all but one show a significant effect of differential population size. All but one sample show an overall tendency for migration to be negative density-dependent; that is, the relative migration rate is greater from larger populations to smaller populations than the reverse.