Human Biology

Published by: Wayne State University Press

translator disclaimer


Human Biology 81(5-6):777-798. 2009
doi: http://dx.doi.org/10.3378/027.081.0621

Human Genetic Diversity and the Nonexistence of Biological Races
No Access

Jeffrey C. Long1 and Rick A. Kittles2

Department of Human Genetics, University of Michigan, Ann Arbor, MI 48109-0618.

National Human Genome Center, Howard University, Washington, D.C. 20060.

Abstract

Sewall Wright's population structure statistic, FST, measured among samples of world populations is often 15% or less. This would indicate that 85% of genetic variation occurs within groups while only 15% can be attributed to allele frequency differences among groups. In this paper, we show that this low value reflects strong biases that result from violating hidden assumptions that define FST. These limitations on FST are demonstrated algebraically and in the context of analyzing dinucleotide repeat allele frequencies for a set of eight loci genotyped in eight human groups and in chimpanzees. In our analyses, estimates of FST. fail to identify important variation. For example, when the analysis includes only humans, FST = 0.119, but adding the chimpanzees increases it only a little, FST = 0.183. By relaxing the underlying statistical assumptions, the results for chimpanzees become consistent with common knowledge, and we see a richer pattern of human genetic diversity. Some human groups are far more diverged than would be implied by standard computations of FST, while other groups are much less diverged. We discuss the relevance of these findings to the application of biological race concepts to humans. Four different race concepts are considered: typological, population, taxonomic, and lineage. Surprisingly, a great deal of genetic variation within groups is consistent with each of these concepts. However, none of the race concepts is compatible with the patterns of variation revealed by our analyses.

Received: July 22, 2002; Revised: May 9, 2003


Literature Cited

Akey, J. M., G. Zhang, K. Shang et al. 2002. Interrogating a high-density SNP map for signatures of natural selection. Genome Research 12:18051814.
American Association of Physical Anthropologists. 1996. AAPA statement on biological aspects of race. Am. J. Phys. Anthropol. 101:569570.
Anderson, T. W. 1973. Asymptotically efficient estimation of covariance matrices with linear structure. Ann. Statistics 1:135141.
Balloux, F., and N. Lugon-Moulin. 2002. The estimation of population differentiation with microsatellite markers. Molecular Ecology 11:155165. CrossRef, PubMed
Bamshad, M. J., S. Wooding, W. S. Watkins et al. 2003. Human population genetic structure and inference of group membership. Am. J. Hum. Genet. 72:578589.
Barbujani, G., A. Magani, E. Minch et al. 1997. An apportionment of human DNA diversity. Proc. Natl. Acad. Sci. (USA) 94:45164519.
Bowcock, A. M., J. R. Kidd, J. Mountain et al. 1991. Drift, admixture, and selection in human evolution: A study with DNA polymorphisms. Proc. Natl. Acad. Sci. (USA) 88:839843.
Bowcock, A. M., A. Ruiz-Linares, J. Tomfohrde et al. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455457. CrossRef, PubMed
Boyd, R., and J. B. Silk. 2000. How Humans Evolved, 2nd ed. New York: W. W. Norton.
Brown, R. A., and G. J. Armelagos. 2001. Apportionment of racial diversity: A review. Evol. Anthropol. 10:3440. CrossRef
Cavalli-Sforza, L. L., and A. Piazza. 1975. Analysis of evolution: Evolutionary rates, independence, and treeness. Theor. Popul. Biol. 37:325.
Cavalli-Sforza, L. L., A. Piazza, P. Menozzi et al. 1988. Reconstruction of human evolution: Bringing together genetic, archeological, and linguistic data. Proc. Natl. Acad. Sci. (USA) 85:60026006. CrossRef, PubMed
Cavalli-Sforza, L. L., P. Menozzi, and A. Piazza. 1994. The History and Geography of Human Genes (abridged paperback edition). Princeton, NJ: Princeton University Press.
Cockerham, C. C. 1969. The variance of gene frequencies. Evolution 23:7284. CrossRef
Cockerham, C. C. 1973. Analyses of gene frequencies. Genetics 74:679700. PubMed
Cockerham, C. C., and B. S. Weir. 1986. Estimation of inbreeding parameters in stratified populations. Ann. Hum. Genet. 50:271281.
Count, G. W. 1950. This is Race. New York: Henry Schumann.
Crow, J. F. 2002. Unequal by nature: A geneticist's perspective on human differences. Daedalus 131:81.
Deka, R., L. Jin, M. D. Shriver et al. 1995. Population genetics of dinucleotide (dC–dA)n [(dG–dT)n polymorphisms in world populations. Am. J. Hum. Genet. 56:461474.
Dobzhansky, T. 1970. Genetics of the Evolutionary Process. New York: Columbia University Press.
Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479491. PubMed
Fredrickson, G. M. 2002. Racism: A Short History. Princeton, NJ: Princeton University Press.
Garza, J. C., M. Slatkin, and N. B. Freimer. 1995. Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol. Biol. Evol. 12:594603. PubMed
Harpending, H., and A. Rogers. 2000. Genetic perspectives on human origins and differentiation. Ann. Rev. Genomics Hum. Genet. 1:361385. CrossRef, PubMed
Hedrick, P. W. 1999. Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313318. CrossRef
Hooton, E. A. 1926. Methods of racial analysis. Science 63:7581.
Jorde, L. B., M. J. Bamshad, W. S. Watkins et al. 1995. Origins and affinities of modern humans: A comparison of mitochondrial and nuclear genetic data. Am. J. Hum. Genet. 57:523538.
Keita, S. O. Y., and R. A. Kitties. 1997. The persistence of racial thinking and the myth of racial divergence. Am. Anthropol. 99:534544.
Lewontin, R. C. 1972. The apportionment of human diversity. Evol. Biol. 6:381398. CrossRef
Lewontin, R. C. 1988. On measures of gametic disequilibrium. Genetics 120:849852.
Lewontin, R. C., and J. Krakauer. 1973. Distribution of gene frequency as a test of the theory of selective neutrality of polymorphism. Genetics 74:175195.
Lieberman, L., and F. L. C. Jackson. 1995. Race and three models of human origin. Am. Anthropol. 97:231242.
Livingstone, F. B. 1963. On the non-existence of human races. Curr. Anthropol. 3:279281.
Mayr, E. 1969. Principles of Systematic Zoology. New York: McGraw-Hill.
Mayr, E. 2002. The biology of race and the concept of equality. Daedalus 131:89.
Morrison, D. F. 1976. Multivariate Statistical Methods. New York: McGraw-Hill.
Nagylaki. T. 1998. Fixation indices in subdivided populations. Genetics 148:13251332.
Nei, M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press.
Nei, M., and A. K. Roychoudhury. 1993. Evolutionary relationships of human populations on a global scale. Mol. Biol. Evol. 10:927943. PubMed
Parra, F. C., R. C. Amado, J. R. Lambertucci et al. 2003. Color and genomic ancestry in Brazilians. Proc. Natl. Acad. Sci. USA 100:177182.
Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945959. PubMed
Quenouille, M. 1956. Notes on bias in estimation. Biometrika 43:253260.
Robertson, A. 1975. Gene frequency distributions as a test of selective neutrality. Genetics 81:775785.
Rosenberg, N. A., J. K. Pritchard, J. L. Weber et al. 2001. Genetic structure of human populations. Science 298:23812385.
Templeton, A. R. 1998. Human races: A genetic and evolutionary perspective. Am. Anthropol. 100: 632650.
Urbanek, M., D. Goldman, and J. C. Long. 1996. The apportionment of dinucleotide repeat diversity in Native Americans and Europeans: A new approach to measuring gene identity reveals asymmetric patterns of divergence. Mol. Biol. Evol. 13:943953.
Weir, B. S. 1996. Genetic Data Analysis. Sunderland, MA: Sinauer Associates, Inc.
Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:13581370. CrossRef
Weir, B. S., and W. G. Hill. 2002. Estimating F-statistics. Annu. Rev. Genet. 36:721750. CrossRef, PubMed
Wilson, E. O., and W. L. Brown. 1953. The subspecies concept and its taxonomic application. Syst. Zool. 2:214220.
Wilson, J. G., M. E. Weale, A. C. Smith et al. 2001. Population genetic structure of variable drug response. Nature Genetics 29:265269. CrossRef, PubMed
Wright, S. 1951. The genetical structure of populations. Annals of Eugenics 15:323354. CrossRef, PubMed
Wright, S. 1965. The interpretation of population structure by F -statistics with special regard to systems of mating. Evolution 19:395420. CrossRef
Wright, S. 1969. Evolution and the Genetics of Populations. Vol. 2, The Theory of Gene Frequencies. Chicago: University of Chicago Press.
Wright, S. 1978. Evolution and the Genetics of Populations. Vol. 4, Variability Within and Among Natural Populations. Chicago: University of Chicago Press.
Yu, N., F.-C. Chen, S. Ota et al. 2002. Larger genetic differences within Africans than between Africans and Eurasians. Genetics 161:269274. PubMed

Cited by

Jason D. Boardman, Benjamin W. Domingue, Jonathan Daw. (2014) What can genes tell us about the relationship between education and health?. Social Science & Medicine.
Online publication date: 1-Aug-2014.
CrossRef
James H. Price, Robert E. Braun, Jagdish Khubchandani, Erica Payton, Prasun Bhattacharjee. (2014) Development of an Attribution of Racial/Ethnic Health Disparities Scale. Journal of Community Health 39, 792-799.
Online publication date: 1-Aug-2014.
CrossRef
Nina G. Jablonski, George Chaplin. (2014) The Evolution of Skin Pigmentation and Hair Texture in People of African Ancestry. Dermatologic Clinics 32, 113-121.
Online publication date: 1-Apr-2014.
CrossRef
Jonathan Marks. (2013) The Nature/Culture of Genetic Facts*. Annual Review of Anthropology 42, 247-267.
Online publication date: 21-Oct-2013.
CrossRef
T. Maruki, S. Kumar, Y. Kim. (2012) Purifying Selection Modulates the Estimates of Population Differentiation and Confounds Genome-Wide Comparisons across Single-Nucleotide Polymorphisms. Molecular Biology and Evolution 29, 3617-3623.
Online publication date: 1-Dec-2012.
CrossRef
Ana V. Diez Roux. (2012) Conceptual Approaches to the Study of Health Disparities. Annual Review of Public Health 33, 41-58.
Online publication date: 21-Apr-2012.
CrossRef
Sarah E. Ali-Khan, Tomasz Krakowski, Rabia Tahir, Abdallah S. Daar. (2011) The use of race, ethnicity and ancestry in human genetic research. The HUGO Journal.
Online publication date: 7-Jul-2011.
CrossRef
click this button to close

Article Views

Article Tools

click this button to open

Citing Articles

 
BioOne is the product of innovative collaboration between scientific societies, libraries, academe and the private sector.
 
21 Dupont Circle NW, Suite 800, Washington, DC 20036 • Phone 202.296.1605 • Fax 202.872.0884
 
Copyright © 2014 BioOne All rights reserved