Extensive nuclear DNA sequence diversity among chimpanzees

Science

Volumn 286, Issue 5442, 1999, Pages 1159-1162

  Kaessmann, Henrik ^a   Wiebe, Victor ^a   Pääbo, Svante ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS DNA;

ARTICLE; CHIMPANZEE; CHROMOSOME XQ; GENETIC DISTANCE; GENETIC VARIABILITY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; DNA; GENOME; GORILLA GORILLA; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PAN PANISCUS; PAN TROGLODYTES; PHYLOGENY; RECOMBINATION, GENETIC; SPECIES SPECIFICITY; VARIATION (GENETICS); X CHROMOSOME;

MAMMALIA; PAN (APE); PAN PANISCUS; PAN TROGLODYTES; PANISCUS; TROGLODYTES;

EID: 0033527718     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.286.5442.1159     Document Type: Article

References (40)

1. A. Whiten et al., Nature 399, 682 (1999).
2. R. E. Bontrop, N. Otting, B. L. Slierendregt, J. S. Lanchbury, Immunol. Rev. 143, 33 (1995).
3. P. Gagneux et al., froc. Natl. Acad. Sci. U.S.A. 96, 5077 (1999).
4. P. A. Morin et al., Science 265, 1193 (1994).
5. C. A. Wise, M. Sraml, D. C. Rubinsztein, S. Easteal, Mol. Biol. Evol. 14, 707 (1997).
6. G. Cooper, D. C. Rubinsztein, W. Amos, Hum. Mol. Genet. 7, 1425 (1998).
7. H. Ellegren, C. R. Primmer, B. C. Sheldon, Nature Genet. 11, 360 (1995); B. Crouau-Roy, S. Service, M. Slatkin, N. Freimer, Hum. Mol. Genet. 5, 1131 (1996).
8. H. Ellegren, C. R. Primmer, B. C. Sheldon, Nature Genet. 11, 360 (1995); B. Crouau-Roy, S. Service, M. Slatkin, N. Freimer, Hum. Mol. Genet. 5, 1131 (1996).
9. H. Kaessmann, F. Heissig, A. von Haeseler, S. Pääbo, Nature Genet. 22, 78 (1999).
10. R. Nagaraja et al., Genome Res. 7, 210 (1997).
11. P. Pamilo and M. Nei, Mol. Biol. Evol. 5, 568 (1988).
12. K. S. Strimmer and A. von Haeseler, Mol. Biol. Evol. 13, 964 (1996). The maximum likelihood tree (Fig. 1) was reconstructed with PUZZLE 4.0 assuming a Tamuro-Nei model with a uniform rate. The clock test was performed with the same program.
13. M. Ruvolo, Mol. Biol. Evol. 14, 248 (1997).
14. W. H. Li and M. Tanimura, Nature 326, 93 (1987).
15. For details on Xq13.3, see supplementary Web information, available at www.sciencemag.org/feature/ data/1043855.shl
16. All sequence positions were determined at least once from each DNA strand, and all variable positions were confirmed by visual inspection of sequence traces.
17. W. O. Hill, in The Chimpanzee, G. H. Bourne, Ed. (Karger, Basel, 1969), pp. 22-49.
18. R. R. Hudson, M. Kreitman, M. Aguadé, Genetics 116, 153 (1987).
19. R. M. Harding et al., Am. J. Hum. Genet. 60, 772 (1997); D. A. Nickerson et at., Nature Genet. 19, 233 (1998); E. E. Harris and J. Hey. Proc. Natl. Acad. Sci. U.S.A. 96, 3320 (1999).
20. R. M. Harding et al., Am. J. Hum. Genet. 60, 772 (1997); D. A. Nickerson et at., Nature Genet. 19, 233 (1998); E. E. Harris and J. Hey. Proc. Natl. Acad. Sci. U.S.A. 96, 3320 (1999).
21. R. M. Harding et al., Am. J. Hum. Genet. 60, 772 (1997); D. A. Nickerson et at., Nature Genet. 19, 233 (1998); E. E. Harris and J. Hey. Proc. Natl. Acad. Sci. U.S.A. 96, 3320 (1999).
22. M. W. Nachman, V. L. Bauer, S. L Crowell, C. F. Aquadro, Genetics 150, 1133 (1998).
23. A. Deinard and K. Kidd, J. Hum. Evol. 36, 687 (1999).
24. A. von Haeseler, A. Sajantila, S. Pääbo, Nature Genet. 14, 135 (1996).
25. L. B. Jorde, M. Bamshad, A. R. Rogers, Bioessays 20, 126 (1998).
26. R. R. Hudson and N. L. Kaplan, Genetics 111, 147 (1985).
27. M. K. Kuhner, J. Yamato, J. Felsenstein, Genetics 140, 1421 (1995). The time to the MRCA of the chimpanzee sequences was estimated with FLUCTUATE (http:// evolution.genetics.washington.edu/lamarc/fluctuate.html). The calculation was performed assuming a global panmictic population of constant population size, the maximum likelihood value of 6, and a generation time of 20 years for both chimpanzees and humans. The program Arlequin (http:// anthropologie.unige.ch/arlequin/ ) was used for calculating Tajima's D [F. Tajima, Genetics 123, 585 (1989)]. Tajima's D was found not to be significantly different from 0 (D = -1.41), thus not rejecting the assumption of constant population size for the chimpanzees.
28. M. K. Kuhner, J. Yamato, J. Felsenstein, Genetics 140, 1421 (1995). The time to the MRCA of the chimpanzee sequences was estimated with FLUCTUATE (http:// evolution.genetics.washington.edu/lamarc/fluctuate.html). The calculation was performed assuming a global panmictic population of constant population size, the maximum likelihood value of 6, and a generation time of 20 years for both chimpanzees and humans. The program Arlequin (http:// anthropologie.unige.ch/arlequin/ ) was used for calculating Tajima's D [F. Tajima, Genetics 123, 585 (1989)]. Tajima's D was found not to be significantly different from 0 (D = -1.41), thus not rejecting the assumption of constant population size for the chimpanzees.
29. V. Reynolds and G. Luscombe, Folia Primatol. 14, 129 (1971).
30. R. M. Nowak, Mammals of the World (John Hopkins Univ. Press, Baltimore, MD, 1991), vol. 1.
31. G. Pesole, E. Sbisa, G. Preparata, C. Saccone, Mol. Biol. Evol. 9, 587 (1992).
32. S. Horai et al., J. Mol. Evol. 35, 32 (1992).
33. W. J. Bailey et al., Mol. Phytogenet. Evol. 1, 97 (1992).
34. H. Vervaecke and L van Elsacker, Mammalia 56, 667 (1992).
35. DNA fragments of 10 kb were amplified from 100 to 200 ng of total genomic DNA with the Boehringer Expand kit and a thermal cycler (MJ Research). Buffer and enzyme concentrations as well as cycling conditions were as recommended by the supplier. One microliter of the product was used to further amplify shorter DNA segments as described (8). Sequencing reactions were pipetted by a Beckman Biomek 2000 robot. Cycling conditions as well as reagent concentrations were as described (8). The sequencing products (0.5 μ) were run on LongReadIR4200 sequencers (LI-COR) with 3.75% RapidGel XL Sol (Amersham Pharmacia) gels. Running conditions were as recommended by the supplier. All sequences, including the orangutan (Fig 1], have been submitted to the European Bioinformatics Institute database (accession numbers: AJ270061 to AJ270095).
36. Most samples were collected from chimpanzee and bonobo individuals for which clear records allowed them to be associated with a particular location in Africa Central African chimpanzees (n = 12) were from the International Center for Medical Research, Gabon. Western chimpanzees were from Sierra Leone (n = 12), zoos, and primate research institutes (n = 5). The eastern chimpanzee was from Gombe, Tanzania. Bonobos, as well as the gorilla and orangutan samples, were from different zoos and primate research institutes. Male sex of all DNA samples was confirmed as described (J. F. Wilson and R. Erlandsson, Biol. Chem. 379, 1287 (1998)].
37. F. Burckhardt, A. von Haeseler, S. Meyer, Nucleic Acids Res. 27, 138 (1999).
38. The BaselmagIRv4.1 software (LICOR) was used for base calling. Sequences and trace data were transferred to the SEQMAN II program (DNASTAR), which was used for sequence assembly. SEQMAN II was also used for the final alignment of the complete sequences and subsequent identification of variable nucleotide positions. The program Arlequin was used for calculation of MPSDs.
39. J. Felsenstein, J. Mol. Evol. 17, 368 (1981). The maximum likelihood tree reconstruction was performed with an ML (no clock) program from the PHYLIP package (http://evolution.genetics.washington.edu/ phylip.html).
40. We thank R. Bontrop, J. Ely, K. Cold, A. Knight, P. Morin, W. Rietschel, C. Roos, A. Stone, O. Takenaka, R. Toder, and J. Wickings for DNA samples; C. Boesch, F. Heissig, P. Morin, and L. Vigilant for constructive discussions and help; and the Deutsche Forschungsgemeinschaft, the Bundesministerium für Bildung, Wissenschaft, Forschung und Technologie, and the Max-Planck-Gesellschaft for financial support.