Genetic evidence for long-term population decline in a Savannah-dwelling primate: Inferences from a hierarchical Bayesian model

Molecular Biology and Evolution

Volumn 19, Issue 11, 2002, Pages 1981-1990

  Storz, Jay F ^a   Beaumont, Mark A ^b   Alberts, Susan C ^c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

^c DUKE UNIVERSITY   (United States)

Author keywords

Baboon; Bayesian inference; Coalescent; Demographic history; Markov chain Monte Carlo; Microsatellite DNA; Papio cynocephalus

Indexed keywords

ANIMAL GENETICS; ARTICLE; BABOON; BAYES THEOREM; CHIMPANZEE; DEMOGRAPHY; ENVIRONMENTAL FACTOR; GENETIC HETEROGENEITY; GEOGRAPHIC DISTRIBUTION; HYPOTHESIS; MATHEMATICAL ANALYSIS; MONTE CARLO METHOD; MUTATION RATE; NONHUMAN; PLEISTOCENE; POPULATION DISTRIBUTION; POPULATION GENETICS; POPULATION SIZE; POPULATION STRUCTURE; PRIMATE; PROBABILITY; SAVANNA; SEASONAL POPULATION DYNAMICS; SPECIES DIFFERENCE; ANIMAL; BIOLOGICAL MODEL; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; MUTAGENESIS; PAPIO; PHYSIOLOGY; POPULATION DENSITY; TIME;

ANIMALIA; MAMMALIA; PAN (APE); PAN TROGLODYTES; PAPIO; PAPIO CYNOCEPHALUS; PAPIO HAMADRYAS; PRIMATES;

ANIMALS; BAYES THEOREM; EVOLUTION, MOLECULAR; GENOTYPE; MARKOV CHAINS; MODELS, BIOLOGICAL; MONTE CARLO METHOD; MUTAGENESIS; PAPIO; POPULATION DENSITY; SELECTION (GENETICS); TIME FACTORS; VARIATION (GENETICS);

EID: 0036856317     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a004022     Document Type: Article

References (85)

1. Altmann, J., S. C. Alberts, S. A. Haines et al. (13 co-authors). 1996. Behavior predicts genetic structure in a wild primate group. Proc. Natl. Acad. Sci. USA 93:5797-5801.
2. Ambrose, S. H. 1998. Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans. J. Hum. Evol. 34:623-651.
3. Awadalla, P., A. Eyre-Walker, and J. Maynard-Smith. 1999. Linkage disequilibrium and recombination in hominoid mitochondrial DNA. Science 286:2524-2525.
4. Barton, N. H. 1995. Linkage and the limits to natural selection. Genetics 140:821-841.
5. Beaumont, M. A. 1999. Detecting population expansion and decline using microsatellites. Genetics 153:2013-2029.
6. Beaumont, M. A., and R. A. Nichols. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B 263:1619-1626.
7. Best, N. G., M. K. Cowles, and S. K. Vines. 1995. CODA Manual Version 0.30. MRC Biostatistics Unit, Cambridge, U.K.
8. Brinkman, B., M. Klintschar, E Neuhuber, J. Huhne, and B. ROLF. 1998. Mutation rate in human microsatellites: Influence of the structure and length of the tandem repeat. Am. J. Hum. Genet. 62:1408-1415.
9. Bruford, M. W., O. Hanotte, J. F. Y. Brookfield, and T. Burke. 1992. Multi- and single-locus DNA fingerprinting. Pp. 225-269 in A. R. Hoelzel, ed. Molecular Analysis of Populations: A Practical Approach. IRL Press, Oxford, U.K.
10. Cambefort, Y., C. Mounie, and P. Colombies. 1976. Chromosome banding patterns of Papio papio. Ann. Genet. 19: 5-9.
11. Chakraborty, R., M. Kimmel, D. N. Stivers, L. J. Davison, and R. Deka. 1997. Relative mutation rates at di-, tri-, and tetranucleotide microsatellite loci. Proc. Natl. Acad. Sci. USA 94:1041-1046.
12. Charlesworth, B., M. T. Morgan, and D. Charlesworth. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
13. Cornuet, J.-M., and G. Luikart. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001-2014.
14. Deka, R., S. Guangyun, D. Smelser et al. (6 co-authors). 1999. Rate and directionality of mutations and effects of allele size constraints at anonymous, gene-associated, and disease-causing trinucleotide loci. Mol. Biol. Evol. 16: 1166-1177.
15. Di Rienzo, A., P. Donnelly, C, Toomajian et al. (8 co-authors). 1998. Heterogeneity of microsatellite mutations within and between loci, and implications for human demographic histories. Genetics 148: 1269-1284.
16. Di Rienzo, A., A. C. Peterson, J. C. Garza, A. M. Valdes, M. Slatkin, and N. B. Freimer. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. USA 91:3166-3170.
17. Donnelly, P. 1999, The coalescent and microsatellite variability. Pp. 116-128 in D. B. Goldstein and C. Schlötterer, eds. Microsatellites: Evolution and Applications. Oxford University Press, Oxford, U.K.
18. Donnelly, P. and S. Tavaré. 1995. Coalescents and genealogical structure under neutrality. Annu. Rev. Genet, 29: 410-421.
19. Ellegren, H. 2000a. Heterogeneous mutation processes in human microsatellite DNA sequences. Nat. Genet. 24:400-402.
20. -. 2000b. Microsatellite mutations in the germline: Implications for evolutionary inference. Trends Genet. 16: 551-558.
21. Emerson, B. C., E. Paradis, and C. Thébaud. 2001. Revealing the demographic histories of species using DNA sequences. Trends. Ecol. Evol. 16:707-716.
22. Estoup, A., and J.-M. Cornuet. 1999. Microsatellite evolution: Inferences from population data. Pp. 49-65 in D. B. Goldstein and C. Schlötterer, eds. Microsatellites: Evolution and Applications. Oxford University Press, Oxford, U.K.
23. Excoffier, L. 1990. Evolution of human mitochondrial DNA: Evidence for departure from a pure neutral model of populations at equilibrium. J. Mol. Evol. 30:125-139.
24. Excoffier, L., and S. Schneider. 1999. Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc. Natl. Acad. Sci. USA 96:10597-10602.
25. Fay, J. C., and C.-I. Wu. 1999. A human population bottleneck can account for the discordance between patterns of mitochondrial and nuclear DNA variation. Mol. Biol. Evol. 16: 1003-1005.
26. Gagneux, P., C. Wills, U. Gerloff, D. Tautz, P. A. Morin, C. Boesch, B. Fruth, G. Hohmann, O. A. Ryder, and D. S. Woodruff. 1999. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl. Acad. Sci. USA 96:5077-5082.
27. Gelman, A., J. B. Carlin, H. S. Stern, and D. B. Rubin. 1995. Bayesian Data Analysis. Chapman and Hall, London, U.K.
28. Goldberg, T. L., and M. Ruvolo. 1997. The geographic apportionment of mitochondrial genetic diversity in East African chimpanzees, Pan troglodytes schweinfurthii, Mol. Biol. Evol. 14:976-984.
29. Goldstein, D. B., A. Ruiz Linares, L. L. Cavalli-Sforza, and M. W. Feldman. 1995. Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA 92:6723-6727.
30. Gonser, R., P. Donnelly, G. Nicholson, and A. Di Rienzo. 2000. Microsatellite mutations and inferences about human demography. Genetics 154:1793-1807.
31. Harpending, H. C., M. A. Batzer, M. Gurven, L. B. Jorde, A. R. Rogers, and S. T. Sherry. 1998. Genetic traces of ancient demography. Proc. Natl. Acad. Sci. USA 95:1961-1967.
32. Harpending, H. C., and A. Rogers. 2000. Genetic perspectives on human origins and differentiation. Annu. Rev. Genomics Hum. Genet. 1:361-385.
33. Hasegawa, M., A. Di Rienzo, and A. C. Wilson. 1993. Toward a more accurate time scale for the human mitochondrial DNA tree. J. Mol. Evol. 37:347-354.
34. Hey, J. 1997. Mitochondrial and nuclear genes present conflicting portraits of human origins. Mol. Biol. Evol. 14:166-172.
35. Hey, J., and E. Harris, 1999. Population bottlenecks and patterns of human polymorphism. Mol. Biol. Evol. 16:1423-1426.
36. Hill, W. G., and A. Robertson. 1966. The effect of linkage on the limits to artificial selection. Genet. Res. 8:269-294.
37. Hudson, R. R. 1990. Gene genealogies and the coalescent process. Oxf. Surv. Evol. Biol. 7:1-44.
38. Ihaka, R., and R. Gentleman. 1996. R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5:299-314.
39. Ingman, M., H. Kaessmann, S. Pääbo, and U. Gyllensten. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408:708-713.
40. Kaplan, N. L., R. R. Hudson, and C. H. Langley. 1989. The "hitchhiking effect" revisited. Genetics 123:887-899.
41. Kayser, M., L. Roewer, M. Hedman et al. (14 co-authors). 2000. Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in father/son pairs. Am. J. Hum. Genet. 66:1580-1588.
42. Klein, R. G. 1989. The Human Career. University of Chicago Press, Chicago.
43. Loader, C. R. 1996. Local likelihood density estimation. Ann. Stat. 24:1602-1618.
44. Maruyama, T., and P. A. Fuerst. 1985. Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675-689.
45. Maynard-Smith, J., and J. Haigh. 1974. The hitchhiking effect of a favorable gene. Genet. Res. 23:23-35.
46. Morin, P. A., P. Mahboubi, S. Wedel, and J. Rogers. 1998. Rapid screening and comparison of human microsatellite markers in baboons: Allele size is conserved, but allele number is not. Genomics 53:12-20.
47. Nachman, M. W. 2001. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet. 17:481-485.
48. Nachman, M. W., V. L. Bauer, S. L. Crowell, and C. F. Aquadro. 1998. DNA variability and recombination rates at X-linked loci in humans. Genetics 150:1133-1141.
49. Nachman, M. W., W. M. Brown, M. Stoneking, and C. F. Aquadro. 1996. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142:953-963.
50. Nei, M., T. Maruyama, and R. Chakraborty. 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1-10.
51. Nordborg, M. 2001. Coalescent theory. Pp. 179-212 in D. J. Balding, M. Bishop, and C. Cannings, eds. Handbook of Statistical Genetics. John Wiley and Sons, New York.
52. Patton, J. L., and M. N. F. Da Silva. 1998. Rivers, refuges, and ridges: The geography of speciation of Amazonian mammals. Pp. 202-213 in D. J. Howard and S. H. Berlocher, eds. Endless Forms: Species and Speciation. Oxford University Press, Oxford, U.K.
53. Payseur, B., and M. W. Nachman. 2000. Microsatellite variation and recombination rate in the human genome. Genetics 156:1285-1298.
54. Pritchard, J. K., M. T. Seielstad, A. Perez-Lezaun, and M. W. Feldman. 1999. Population growth of human Y chromosomes: A study of Y chromosome microsatellites. Mol. Biol. Evol. 16:1791-1798.
55. Przeworski, M., R. R. Hudson, and A. Di Rienzo. 2000. Adjusting the focus on human variation. Trends Genet. 16:296-302.
56. Rampino, M. R., and S. Self. 1992. Volcanic winter and accelerated glaciation following the Toba super-eruption. Nature 359:50-52.
57. -. 1993. Bottleneck in human evolution and the Toba eruption. Science 262:1955.
58. Relethford, J. H. 2001. Genetic history of the human species. Pp. 813-846 in D. J. Balding, M. Bishop, and C. Cannings, eds. Handbook of Statistical Genetics. John Wiley and Sons, New York.
59. Renwick, A., L. Davison, H. Spratt, J. P. King, and M. Kimmel. 2001. DNA dinucleotide evolution in humans: Fitting theory to facts. Genetics 159:737-747.
60. Rogers, A. R. 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49:608-615.
61. -. 1996. Mitochondrial mismatch analysis is insensitive to the mutational process. Mol. Biol. Evol. 13:895-902.
62. Rogers, A. R., and H. C. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9:552-569.
63. Rogers, A. R., and L. B. Jorde. 1995. Genetic evidence on modern human origins. Hum. Biol. 67:1-36.
64. Rogers, J., M. C. Mahaney, S. M. Witte et al. (17 co-authors). 2000. A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms. Genomics 67:237-247.
65. Ruvolo, M. 1996. A new approach to studying modern human origins: Hypothesis testing with coalescence time distributions. Mol. Phylogenet. Evol. 5:202-219.
66. Samuels, A., and J. Altmann. 1991. Baboons of the Amboseli basin: Demographic stability and change. Int. J. Primatol. 12:1-19.
67. Schlötterer, C. 2000. Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365-371.
68. Sherry, S., A. R. Rogers, H. C. Harpending, H. Soodyall, T. Jenkins, and M. Stoneking. 1994. Mismatch distributions of mtDNA reveal recent human population expansions. Hum. Biol. 66:761-775.
69. Stephens, M. 2001. Inference under the coalescent. Pp. 213-238 in D. J. Balding, M. Bishop, and C. Cannings, eds. Handbook of Statistical Genetics. John Wiley and Sons, New York.
70. Stephens, M., and P. Donnelly. 2000. Inference in molecular population genetics. J. Roy. Stat. Soc. B 62:605-635.
71. Storz, J. F., and M. A. Beaumont. 2002. Testing for genetic evidence of population expansion and contraction: An empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154-166.
72. Storz, J. F., U. Ramakrishnan, and S. C. Alberts. 2001. Determinants of effective population size for loci with different modes of inheritance. J. Hered. 92:497-502.
73. -. 2002. Genetic effective size of a wild primate population: Influence of current and historical demography. Evolution 56:817-829.
74. Tajima, F. 1989a. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
75. -. 1989b. The effect of change in population size on DNA polymorphism. Genetics 123:597-601.
76. Thomson, R., J. K. Pritchard, P. D. Shen, P. J. Oefner, and M. W. Feldman. 2000. Recent common ancestry of human Y chromosomes: Evidence from DNA sequence data. Proc. Natl. Acad. Sci. USA 97:7360-7365.
77. Vitalis, R., K. Dawson, and P. Boursot. 2001. Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811-1823.
78. Wakeley, J. 1999. Nonequilibrium migration in human history. Genetics 153:1863-1871.
79. Wakeley, J., R. Nielsen, S. N. Liu-cordero, and K. Ardlie. 2001. The discovery of single-nucleotide polymorphisms - And inferences about human demographic history. Am. J. Hum. Genet. 69:1332-1347.
80. Wall, J. D., and M. Przeworski. 2000. When did the human population size start increasing? Genetics 155:1865-1874.
81. Watson, E., P. Forster, M. Richards, and N.-J. Bandelt. 1997. Mitochondrial footprints of human expansions in Africa. Am. J. Hum. Genet. 61:691-704.
82. Watterson, G. A. 1984. Allele frequencies after a bottleneck. Theor. Popul. Biol. 26:387-407.
83. Wiehe, T. 1998. The effect of selective sweeps on the variance of the allele distribution of a linked multiallele locus: Hitch-hiking of microsatellites. Theor. Popul. Biol. 53:272-283.
84. Wilson, I. J., and D. J. Balding. 1998. Genealogical inference from microsatellite data. Genetics 150:499-510.
85. Wise, C. A., M. Sraml, and S. Easteal. 1998. Departure from neutrality at the mitochondrial NADH dehydrogenase sub-unit 2 gene in humans, but not in chimpanzees. Genetics 148:409-421.