Skip to main content
NCBI home page
American Journal of Human Genetics logoLink to American Journal of Human Genetics
. 1988 Nov;43(5):709–725.

Population amalgamation and genetic variation: observations on artificially agglomerated tribal populations of Central and South America.

R Chakraborty 1, P E Smouse 1, J V Neel 1
PMCID: PMC1715540  PMID: 3189334

Abstract

The interpretation of data on genetic variation with regard to the relative roles of different evolutionary factors that produce and maintain genetic variation depends critically on our assumptions concerning effective population size and the level of migration between neighboring populations. In humans, recent population growth and movements of specific ethnic groups across wide geographic areas mean that any theory based on assumptions of constant population size and absence of substructure is generally untenable. We examine the effects of population subdivision on the pattern of protein genetic variation in a total sample drawn from an artificial agglomerate of 12 tribal populations of Central and South America, analyzing the pooled sample as though it were a single population. Several striking findings emerge. (1) Mean heterozygosity is not sensitive to agglomeration, but the number of different alleles (allele count) is inflated, relative to neutral mutation/drift/equilibrium expectation. (2) The inflation is most serious for rare alleles, especially those which originally occurred as tribally restricted "private" polymorphisms. (3) The degree of inflation is an increasing function of both the number of populations encompassed by the sample and of the genetic divergence among them. (4) Treating an agglomerated population as though it were a panmictic unit of long standing can lead to serious biases in estimates of mutation rates, selection pressures, and effective population sizes. Current DNA studies indicate the presence of numerous genetic variants in human populations. The findings and conclusions of this paper are all fully applicable to the study of genetic variation at the DNA level as well.

Full text

PDF
709

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrantes R., Smouse P. E., Neel J. V., Mohrenweiser H. W., Gershowitz H. Migration and genetic infrastructure of the Central American Guaymi and their affinities with other tribal groups. Am J Phys Anthropol. 1982 Jun;58(2):201–214. doi: 10.1002/ajpa.1330580213. [DOI] [PubMed] [Google Scholar]
  2. Chagnon N. A., Neel J. V., Weitkamp L., Gershowitz H., Ayres M. The influence of cultural factors on the demography and pattern of gene flow from the Makiritare to the Yanomama Indians. Am J Phys Anthropol. 1970 May;32(3):339–349. doi: 10.1002/ajpa.1330320304. [DOI] [PubMed] [Google Scholar]
  3. Chakraborty R., Fuerst P. A., Nei M. Statistical Studies on Protein Polymorphism in Natural Populations. III. Distribution of Allele Frequencies and the Number of Alleles per Locus. Genetics. 1980 Apr;94(4):1039–1063. doi: 10.1093/genetics/94.4.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chakraborty R. Number of independent genes examined in family surveys and its effect on gene frequency estimation. Am J Hum Genet. 1978 Sep;30(5):550–552. [PMC free article] [PubMed] [Google Scholar]
  5. Chakravarti A., Buetow K. H., Antonarakis S. E., Waber P. G., Boehm C. D., Kazazian H. H. Nonuniform recombination within the human beta-globin gene cluster. Am J Hum Genet. 1984 Nov;36(6):1239–1258. [PMC free article] [PubMed] [Google Scholar]
  6. Chakravarti A., Elbein S. C., Permutt M. A. Evidence for increased recombination near the human insulin gene: implication for disease association studies. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1045–1049. doi: 10.1073/pnas.83.4.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ewens W. J., Gillespie J. H. Some simulation results for the neutral allele model, with interpretations. Theor Popul Biol. 1974 Aug;6(1):35–57. doi: 10.1016/0040-5809(74)90030-6. [DOI] [PubMed] [Google Scholar]
  8. Ewens W. J. The sampling theory of selectively neutral alleles. Theor Popul Biol. 1972 Mar;3(1):87–112. doi: 10.1016/0040-5809(72)90035-4. [DOI] [PubMed] [Google Scholar]
  9. Gershowitz H., Neel J. V. The immunoglobulin allotypes (Gm and Km) of twelve Indian tribes of Central and South America. Am J Phys Anthropol. 1978 Sep;49(3):289–301. doi: 10.1002/ajpa.1330490302. [DOI] [PubMed] [Google Scholar]
  10. Harris H., Hopkinson D. A., Robson E. B. The incidence of rare alleles determining electrophoretic variants: data on 43 enzyme loci in man. Ann Hum Genet. 1974 Jan;37(3):237–253. doi: 10.1111/j.1469-1809.1974.tb01832.x. [DOI] [PubMed] [Google Scholar]
  11. KIMURA M., CROW J. F. THE NUMBER OF ALLELES THAT CAN BE MAINTAINED IN A FINITE POPULATION. Genetics. 1964 Apr;49:725–738. doi: 10.1093/genetics/49.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Long J. C., Smouse P. E. Intertribal gene flow between the Ye'cuana and Yanomama: genetic analysis of an admixed village. Am J Phys Anthropol. 1983 Aug;61(4):411–422. doi: 10.1002/ajpa.1330610403. [DOI] [PubMed] [Google Scholar]
  13. Mestriner M. A., Simoes A. L., Salzano F. M. New studies on the esterase D polymorphism in South American Indians. Am J Phys Anthropol. 1980 Jan;52(1):95–101. doi: 10.1002/ajpa.1330520112. [DOI] [PubMed] [Google Scholar]
  14. Mohrenweiser H., Neel J. V., Mestriner M. A., Salzano F. M., Migliazza E., Simões A. L., Yoshihara C. M. Electrophoretic variants in three Amerindian tribes: the Baniwa, Kanamari, and Central Pano of western Brazil. Am J Phys Anthropol. 1979 Feb;50(2):237–246. doi: 10.1002/ajpa.1330500212. [DOI] [PubMed] [Google Scholar]
  15. Murray J. C., Mills K. A., Demopulos C. M., Hornung S., Motulsky A. G. Linkage disequilibrium and evolutionary relationships of DNA variants (restriction enzyme fragment length polymorphisms) at the serum albumin locus. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3486–3490. doi: 10.1073/pnas.81.11.3486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Neel J. V. "Private" genetic variants and the frequency of mutation among South American Indians. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3311–3315. doi: 10.1073/pnas.70.12.3311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Neel J. V., Gershowitz H., Mohrenweiser H. W., Amos B., Kostyu D. D., Salzano F. M., Mestriner M. A., Lawrence D., Simões A. L., Smouse P. E. Genetic studies on the Ticuna, an enigmatic tribe of Central Amazonas. Ann Hum Genet. 1980 Jul;44(Pt 1):37–54. doi: 10.1111/j.1469-1809.1980.tb00944.x. [DOI] [PubMed] [Google Scholar]
  18. Neel J. V., Gershowitz H., Spielman R. S., Migliazza E. C., Salzano F. M., Oliver W. J. Genetic studies of the Macushi and Wapishana Indians. II. Data on 12 genetic polymorphisms of the red cell and serum proteins: gene flor between the tribes. Hum Genet. 1977 Jun 30;37(2):207–219. doi: 10.1007/BF00393584. [DOI] [PubMed] [Google Scholar]
  19. Neel J. V., Mohrenweiser H. W., Rothman E. D., Naidu J. M. A revised indirect estimate of mutation rates in Amerindians. Am J Hum Genet. 1986 May;38(5):649–666. [PMC free article] [PubMed] [Google Scholar]
  20. Neel J. V., Rothman E. D. Indirect estimates of mutation rates in tribal Amerindians. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5585–5588. doi: 10.1073/pnas.75.11.5585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Neel J. V., Satoh C., Goriki K., Fujita M., Takahashi N., Asakawa J., Hazama R. The rate with which spontaneous mutation alters the electrophoretic mobility of polypeptides. Proc Natl Acad Sci U S A. 1986 Jan;83(2):389–393. doi: 10.1073/pnas.83.2.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Neel J. V., Tanis R. J., Migliazza E. C., Spielman R. S., Salzano F., Oliver W. J., Morrow M., Bachofer S. Genetic studies of the Macushi and Wapishana Indians. I. Rare genetic variants and a "private polymorphism' of esterase A. Hum Genet. 1977 Apr 7;36(1):81–107. doi: 10.1007/BF00390440. [DOI] [PubMed] [Google Scholar]
  23. Neel J. V., Thompson E. A. Founder effect and number of private polymorphisms observed in Amerindian tribes. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1904–1908. doi: 10.1073/pnas.75.4.1904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Neel J. V., Ueda N., Satoh C., Ferrell R. E., Tanis R. J., Hamilton H. B. The frequency in Japanese of genetic variants of 22 proteins. V. Summary and comparison with data on Caucasians from the British Isles. Ann Hum Genet. 1978 May;41(4):429–441. doi: 10.1111/j.1469-1809.1978.tb00913.x. [DOI] [PubMed] [Google Scholar]
  25. Nei M., Roychoudhury A. K. Sampling variances of heterozygosity and genetic distance. Genetics. 1974 Feb;76(2):379–390. doi: 10.1093/genetics/76.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nei M., Tajima F., Tateno Y. Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol. 1983;19(2):153–170. doi: 10.1007/BF02300753. [DOI] [PubMed] [Google Scholar]
  27. Ohta T. Role of very slightly deleterious mutations in molecular evolution and polymorphism. Theor Popul Biol. 1976 Dec;10(3):254–275. doi: 10.1016/0040-5809(76)90019-8. [DOI] [PubMed] [Google Scholar]
  28. Salzano F. M., Gershowitz H., Junqueira P. C., Woodall J. P., Black F. L., Hierholzer W. Blood groups and H-Le a salivary secretion of Brazilian Cayapo Indians. Am J Phys Anthropol. 1972 May;36(3):417–425. doi: 10.1002/ajpa.1330360313. [DOI] [PubMed] [Google Scholar]
  29. Salzano F. M., Gershowitz H., Mohrenweiser H., Neel J. V., Smouse P. E., Mestriner M. A., Weimer T. A., Franco M. H., Simões A. L., Constans J. Gene flow across tribal barriers and its effect among the Amazonian Içana river Indians. Am J Phys Anthropol. 1986 Jan;69(1):3–14. doi: 10.1002/ajpa.1330690103. [DOI] [PubMed] [Google Scholar]
  30. Salzano F. M., Mohrenweiser H., Gershowitz H., Neel J. V., Mestriner M. A., Simões A. L., Constans J., De Melo e Freitas M. J. New studies on the Macushi Indians of northern Brazil. Ann Hum Biol. 1984 Jul-Aug;11(4):337–350. doi: 10.1080/03014468400007241. [DOI] [PubMed] [Google Scholar]
  31. Salzano F. M., Neel J. V., Gershowitz H., Migliazza E. C. Intra and intertribal genetic variation within a linguistic group: the Ge-speaking indians of Brazil. Am J Phys Anthropol. 1977 Sep;47(2):337–347. doi: 10.1002/ajpa.1330470214. [DOI] [PubMed] [Google Scholar]
  32. Salzano F. M., Pages F., Neel J. V., Gershowitz H., Tanis R. J., Moreno R., Franco M. H. Unusual blood genetic characteristics among the Ayoreo Indians of Bolivia and Paraguay. Hum Biol. 1978 May;50(2):121–136. [PubMed] [Google Scholar]
  33. Singh R. S., Rhomberg L. R. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. I. Estimates of Gene Flow from Rare Alleles. Genetics. 1987 Feb;115(2):313–322. doi: 10.1093/genetics/115.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Spielman R. S., Migliazza E. C., Neel J. V. Regional linguistic and genetic differences among Yanomama indians. Science. 1974 May 10;184(4137):637–644. doi: 10.1126/science.184.4137.637. [DOI] [PubMed] [Google Scholar]
  35. Strobeck C. Average number of nucleotide differences in a sample from a single subpopulation: a test for population subdivision. Genetics. 1987 Sep;117(1):149–153. doi: 10.1093/genetics/117.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thompson E. A., Neel J. V. Probability of founder effect in a tribal population. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1442–1445. doi: 10.1073/pnas.75.3.1442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ward R. H., Gershowitz H., Layrisse M., Neel J. V. The genetic structure of a tribal population, the Yanomama Indians XI. Gene frequencies for 10 blood groups and the ABH-Le secretor traits in the Yanomama and their neighbors; the uniqueness of the tribe. Am J Hum Genet. 1975 Jan;27(1):1–30. [PMC free article] [PubMed] [Google Scholar]
  38. Watterson G. A. An analysis of multi-allelic data. Genetics. 1978 Jan;88(1):171–179. doi: 10.1093/genetics/88.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from American Journal of Human Genetics are provided here courtesy of American Society of Human Genetics

RESOURCES