Patterns of Human Diversity, within and among Continents, Inferred from Biallelic DNA Polymorphisms

Abstract

Previous studies have reported that about 85% of human diversity at Short Tandem Repeat (STR) and Restriction Fragment Length Polymorphism (RFLP) autosomal loci is due to differences between individuals of the same population, whereas differences among continental groups account for only 10% of the overall genetic variance. These findings conflict with popular notions of distinct and relatively homogeneous human races, and may also call into question the apparent usefulness of ethnic classification in, for example, medical diagnostics. Here, we present new data on 21 Alu insertions in 32 populations. We analyze these data along with three other large, globally dispersed data sets consisting of apparently neutral biallelic nuclear markers, as well as with a ␤-globin data set possibly subject to selection. We confirm the previous results for the autosomal data, and find a higher diversity among continents for Y-chromosome loci. We also extend the analyses to address two questions: (1) whether differences between continental groups, although small, are nevertheless large enough to confidently assign individuals to their continent on the basis of their genotypes; (2) whether the observed genotypes naturally cluster into continental or population groups when the sample source location is ignored. Using a range of statistical methods, we show that classification errors are at best around 30% for autosomal biallelic polymorphisms and 27% for the Y chromosome. Two data sets suggest the existence of three and four major groups of genotypes worldwide, respectively, and the two groupings are inconsistent. These results suggest that, at random biallelic loci, there is little evidence, if any, of a clear subdivision of humans into biologically defined groups.In various areas of applied genetics, it is customary to regard the human species as divided in distinct and objectively recognizable groups. Forensic scientists compare DNA profiles from the place of a crime with databases from the general population, usually grouped into broad racial categories (for instance, African-American, European-American, Asian, and Hispanic), to estimate the probability that an unrelated individual would have the identical DNA profile. The markers chosen for DNA profiling are considered to be essentially uniform across populations of the same category. Although the existence of problems with group definition has been acknowledged (e.g., Weir 2001), the fact that some individuals may not be easy to allocate to any such group is usually regarded as unimportant (National Research Council 1992;Lander and Budowle 1994;Morton 1994;Roeder 1994;Gill and Evett 1995). In clinical practice, a correlation of racial affiliation, as assessed from skin color, facial characteristics, hair texture, and so forth, with disease pathology and drug response is widely believed to exist. A PubMed search with the keywords "human races" (January 10, 2002) In contrast, population studies have suggested that genetic variation is essentially continuous through space amon...

A Tale of Aborigines, Conquerors and Slaves: Alu Insertion Polymorphisms and the Peopling of Canary Islands

“…In four heterozygous individuals (one from Tenerife, one from Gran Canaria and two from Fuerteventura) a larger-than-expected Alu insertion was found. The sequences of these alleles correspond to an Alu insertion within a pre-existing PAI, which has previously been found in two Basque and one northern Moroccan chromosomes from a broad set of populations worldwide (Comas et al 2001, Romualdi et al 2002, Bamshad et al 2003. Its presence in the current Canarians evidences the clear and strong relationship of this population with those from Iberia and Northwestern Africa.…”

“…Polymorphic Alu insertions (PAI), scattered throughout the human genome, occur as unique events in our evolution and are apparently selectively neutral (Batzer & Deininger, 2002). These markers have been used extensively for population structure and evolution, both at global (Bazter et al 1996;Antúnez-de-Mayolo et al 2002;Romualdi et al 2002;Bamshad et al 2003) and regional levels (Majumder et al 1999;Comas et al 2000Comas et al , 2004Martínez de Pancorbo et al 2001;Nasidze et al 2001). In this study, we genotyped 10 PAI in samples from the seven main islands of the Canarian archipelago, in order to fill in the gaps in autosomal studies.…”

Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males

“…This problem is exacerbated for Y chromosomes because they lack sequence diversity 5 . To accommodate this difficulty, Y-chromosome researchers have adopted a strategy [6][7][8][9] to estimate levels of between-group variation using single-nucleotide polymorphisms (SNPs) discovered in small panels of globally diverse males and then genotyped in much larger population samples (e.g., the global data set 10 analyzed in ref. 1).…”

Genetic variation, classification and 'race'

“…At least two such studies have concluded that the observed clustering patterns do not correspond well to the subjects' geographic origins or 'ethnic labels' 30,31 . These studies, however, were based on only several dozen or fewer loci, and a small sample of unselected loci does not typically provide sufficient power to detect population structure when individuals are analyzed 6,32 .…”