Chromosomal speciation and molecular divergence - Accelerated evolution in rearranged chromosomes

Science

Volumn 300, Issue 5617, 2003, Pages 321-324

  Navarro, Arcadi ^a   Barton, Nick H ^b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA SEQUENCES; GENES; PROTEINS;

CHROMOSOMAL SPECIATION;

CHROMOSOMES;

GENOMIC DNA; NUCLEOTIDE;

CHROMOSOME; EVOLUTION; POLYMORPHISM; PRIMATE; SPECIATION (BIOLOGY);

ANIMAL GENETICS; ARTICLE; CHIMPANZEE; CHROMOSOME INVERSION; CHROMOSOME REARRANGEMENT; DNA SEQUENCE; EVOLUTION; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SPECIES DIFFERENTIATION;

ALLELES; AMINO ACID SUBSTITUTION; ANIMALS; CHROMOSOMES, HUMAN; CHROMOSOMES, MAMMALIAN; EVOLUTION; EVOLUTION, MOLECULAR; GENETICS, POPULATION; HOMINIDAE; HUMANS; INVERSION, CHROMOSOME; KARYOTYPING; MUTATION; PAN TROGLODYTES; PROTEINS; RECOMBINATION, GENETIC; REPRODUCTION; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

ANIMALIA; PAN (APE); PAN TROGLODYTES; PRIMATES; VERTEBRATA;

EID: 0037432734     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.1080600     Document Type: Article

References (45)

1. H. King, Species Evolution (Cambridge Univ. Press., Cambridge, 1993).
2. F. Spirito, in Endless Forms D. J. Howard, S. H. Berlocher, Eds. (Oxford Univ. Press, New York, 2000), pp. 320-329.
3. L. H. Rieseberg, Trends Ecol. Evol. 16, 351 (2001),
4. M. A. F. Noor, K. L Grams, L A. Bertucci, J. Reiland, Proc. Natl. Acad. Sci. U.S.A. 98, 12084 (2001).
5. C. A. Machado, R. M. Kliman, J. A. Markert, J. Hey, Mol. Biol. Evol. 19, 472 (2002).
6. D. Ortiz-Barrientos, J. Reiland, J. Hey, M. A. Noor, Genetica 116, 167 (2002).
7. A. Navarro, N. H. Barton, Evolution 57, 447 (2003).
8. H. A. Orr, Genetics 144, 1331 (1997).
9. D. N. Janczewski, D. Goldman, S. J. O'Brien, J. Hered. 81, 375 (1990).
10. S. Consigliere, R. Stanyon, U. Koehler, G. Agoramoorthy, J. Wienberg, Chromosome Res. 4, 264 (1996).
11. J. J. Yunis, O. Prakash, Science 215, 1525 (1982).
12. D. Haig, Philos. Trans. R. Soc. London Ser. B Biol. Sci. 354, 1447 (1999).
13. J. Vieira, B. F. McAllister, B. Charlesworth, Genetics 158, 279 (2001).
14. R. Hudson, Oxford Surv. Evol. Biol. 7, 1 (1990).
15. M. Kimura, The Neutral Theory of Molecular Evolution (Cambridge Univ. Press. Cambridge, 1983).
16. As shown in supporting online material, the measures had different sources. Most of them (86) were obtained by analyzing sequences retrieved from Gen-Bank; 17 by reanalyzing sequences provided by authors, and 12 directly from the literature. Whenever possible, literature data or sequences provided by authors were checked against GenBank sequences. When different sources provided different divergence estimates for the same gene or when more than one allele was available, the pairs of sequences with the smallest distances were selected for analysis, so the most ancestral variants were used. Genes with no divergence or for which ancestral polymorphism has been reported were excluded from this analysis. Also, to avoid redundant information, duplicated genes in tandem for which gene conversion has been reported were also excluded.
17. W. H. Li, J. Mol. Evol. 36, 96 (1993). The maximum likelihood method implemented in the package PAML (44) performs better than Li's method, which we use here. Yang's method could not be used with our full data set, because the divergence measures obtained directly from the literature used Li's method. The methods, however, should not produce different results for such a short distance as the time separating humans and chimpanzees. This was confirmed by repeating our primary calculations using PAML on the reduced data set. The results obtained in this way did not differ from the ones presented here.
18. X. Xia, Z. Xie, J. Hered. 92, 371 (2001).
19. F. C. Chen, W. H, Li, Am. J. Hum. Genet. 68, 444 (2001).
20. The cytological positions of the breakpoints of the chromosomal changes separating the genomes of humans and chimpanzees (see table 52) and a classification of chromosomal regions were determined as previously described (11, 12).
21. S depends on the proportion in which gene flow is reduced, whereas incompatibilities leading to higher KA can only be established below a given threshold of gene flow.
22. S. Yi, D. L. Ellsworth, W. H. Li, Mol. Biol. Evol. 19, 2191 (2002).
23. I. Ebersberger, D. Metzler, C. Schwarz, S. Paabo, Am. J. Hum. Genet. 70, 1490 (2002).
24. From table 1 of (22), we obtained a set of 45 values of the number of nucleotide substitutions per 100 sites, K, between human and chimpanzee sequences, based on 447,330 bp of noncoding, nonrepetitive sequences from different chromosomes. S. Yi kindly provided the amounts of GC for these data. Second, I. Ebersberger kindly provided the K values and amounts of GC for the set of 8859 sequence pairs encompassing 1,944,162 bp of sequences from all the genome that were analyzed in (23).
25. M. J. Lercher, E. J. B. Williams, L. D. Hurst, Mol. Biol. Evol. 18, 2032 (2001).
26. G. Bernardi, Gene 241, 3 (2000).
27. E. J. B. Williams, L. D. Hurst, Nature 407, 900 (2000).
28. -, Mol. Biol. Evol. 19, 1395 (2002).
29. J. Castresana, Nucl. Acids Res. 30, 1751 (2002).
30. Their GC4 content was ascertained by means of DNAsp by J. Rozas and R. Rozas [Bioinformatics 15, 174 (1999)]. Because the ancestral sequence is not available, the average GC4 content of the two sequences was used.
31. A. Eyre-Walker, Proc. R. Soc. London Ser. B Biol. Sci. 252, 237 (1993).
32. A. Kong et al., Nature Genet. 31, 241 (2002).
33. M. Brunet et al., Nature 418, 145 (2002).
34. P. Vignaud et al., Nature 418, 152 (2002).
35. M. Przeworski, R. R. Hudson, A. Di Rienzo, Trends Genet. 16, 296 (2000).
36. J. C. Stephens et al., Science 293, 489 (2001).
37. w) and of the deviation from the frequency spectrum expected under neutrality (Tajima's D) for 292 autosomal genes from the data set of variability measures in (36).
38. P. Andolfatto, F. Depaulis, A. Navarro, Genet. Res. 77, 1 (2001).
39. M. W. Fitch, Biochem. Genet. 5, 231 (1971).
40. P. Lopez, D. Casane, H. Philippe, Mol. Biol. Evol. 19, 1 (2002).
41. G. S. Van Doom, P. C. Luttikhuizen, F. J. Weissing, Proc. R. Soc. London Ser. B 268, 2155 (2001).
42. M. Wallis, J. Mol. Evol. 53, 10 (2001).
43. T. Johnson, N. H. Barton, Genetics 162, 395 (2002).
44. Z. Yang, Phylogenetic Analysis by Maximum Likelihood (PAML), version 3.13a (University College London, London, 2002); available at http://abacus. gene.ucl.ac.uk/software/paml.html
45. We thank A. Andrés, J. Bertranpetit, F. Calafell, J. Castresana, B. Charlesworth, D. Charlesworth, F. Depaulis, T. Johnson, P. Keightley, H. Laayouni, K. Lythgoe, G. Marais, X. Maside, T. Vines, and the staff of Biomedical Systems Group for helpful discussion and criticism. We are also grateful to F.-C. Chen, I. Ebersberger, A. Eyre-Walker, J. Fay, P. Keightley, W.-H. Li, S. Paabo and S. Yi for kindly making data available. The detailed comments of J. Bertranpetit, D. Charlesworth, B. Charlesworth and F. Depaulis greatly improved a previous version of the manuscript. This research was funded by the National Environmental Research Council (UK), Ministerio de Ciencia y Tecnologia (Spain, BMC 2001-0772), and the Ramón y Cajal Program (Spain).