Convergently recruited nuclear transport retrogenes are male biased in expression and evolving under positive selection in drosophila

Genetics

Volumn 184, Issue 4, 2010, Pages 1067-1076

  Tracy, Charles ^a   Río, Javier ^a   Motiwale, Mansi ^a   Christensen, Shawn M ^a   Betrán, Esther ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; EVOLUTIONARY ADAPTATION; FEMALE; GENDER BIAS; GENE DUPLICATION; GENE EXPRESSION; GENE INACTIVATION; GENOMICS; MALE; MEIOSIS; NATURAL SELECTION; NONHUMAN; NUCLEAR IMPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEX DIFFERENCE; SPERMATOGENESIS; X CHROMOSOME; ALLELE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC TRANSCRIPTION; GENETICS; GENOME; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; SEXUAL DEVELOPMENT; TIME;

DROSOPHILA ANANASSAE; DROSOPHILA ATRIPEX; DROSOPHILA GRIMSHAWI; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; DROSOPHILA YAKUBA; MAMMALIA;

DROSOPHILA PROTEIN; NTF 2 PROTEIN, DROSOPHILA; NTF-2 PROTEIN, DROSOPHILA; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; RAN PROTEIN;

ALLELES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; FEMALE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENOME, INSECT; HUMANS; MALE; MOLECULAR SEQUENCE DATA; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; POLYMORPHISM, GENETIC; RAN GTP-BINDING PROTEIN; SELECTION, GENETIC; SEX CHARACTERISTICS; TIME FACTORS; TRANSCRIPTION, GENETIC; X CHROMOSOME;

EID: 77955903376     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.113522     Document Type: Article

References (50)

1. AKASHI, H., 1995 Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139: 1067-1076.
2. BAI, Y., C. CASOLA, C. FESCHOTTE and E. BETRÁN, 2007 Comparative genomics reveals a constant rate of origination and convergent acquisition of functional retrogenes in Drosophila. Genome Biol. 8: R11.
3. BEGUN, D. J., and H. A. LINDFORS, 2005 Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila. Mol. Biol. Evol. 22: 2010-2021.
4. BETRÁN, E., and M. LONG, 2003 Dntf-2r: a young Drosophila retroposed gene with specific male expression under positive Darwinian selection. Genetics 164: 977-988.
5. BETRÁN, E., K. THORNTON and M. LONG, 2002 Retroposed new genes out of the X in Drosophila. Genome Res. 12: 1854-1859.
6. BRADLEY, J., A. BALTUS, H. SKALETSKY, M. ROYCE-TOLLAND, K. DEWAR et al., 2004 An X-to-autosome retrogene is required for spermatogenesis in mice. Nat. Genet. 36: 872-876.
7. BROSIUS, J., 1991 Retroposons-seeds of evolution. Science 251: 753.
8. BURT, A., and R. TRIVERS, 2006 Genes in Conflict. The Biology of Selfish Genetic Elements. Harvard University Press, Cambridge, MA.
9. CHARLESWORTH, B., J. A. COYNE and N. H. BARTON, 1987 The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130: 113-146.
10. CHINTAPALLI, V. R., J. WANG and J. A. DOW, 2007 Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39: 715-720.
11. CHIPPINDALE, A. K., J. R. GIBSON and W. R. RICE, 2001 Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl. Acad. Sci. USA 98: 1671-1675.
12. CLARK, A. G., M. B. EISEN, D. R. SMITH, C. M. BERGMAN, B. OLIVER et al., 2007 Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
13. EMERSON, J. J., H. KAESSMANN, E. BETRÁN and M. LONG, 2004 Extensive gene traffic on the mammalian X Chromosome. Science 303: 537-540.
14. FAY, J. C., and C. I. WU, 2000 Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
15. HENSE, W., J. F. BAINES and J. PARSCH, 2007 X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol. 5: e273.
16. HOLLOCHER, H., C. T. TING, M. L. WU and C. I. WU, 1997 Incipient speciation by sexual isolation in Drosophila melanogaster: variation in mating preference and correlation between sexes. Evolution 51: 1175-1181.
17. KINGAN, S. B., D. GARRIGAN and D. L. HARTL, 2009 Recurrent selection on the Winters sex-ratio genes in Drosophila simulans. Genetics 184: 253-265.
18. KOSAKOVSKY POND, S. L., and S. D. FROST, 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22: 1208-1222.
19. KUSANO, A., C. STABER and B. GANETZKY, 2002 Segregation distortion induced by wild-type RanGAP in Drosophila. Proc. Natl. Acad. Sci. USA 99: 6866-6870.
20. KUSANO, A., C. STABER, H. Y. CHAN and B. GANETZKY, 2003 Closing the (Ran)GAP on segregation distortion in Drosophila. Bioessays 25: 108-115.
21. LARRACUENTE, A. M., T. B. SACKTON, A. J. GREENBERG, A. WONG, N. D. SINGH et al., 2008 Evolution of protein-coding genes in Drosophila. Trends Genet. 24: 114-123.
22. LIBRADO, P., and J. ROZAS, 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
23. LIFSCHYTZ, E., and D. L. LINDSLEY, 1972 The role of X-chromosome inactivation during spermatogenesis. Proc. Natl. Acad. Sci. USA 69: 182-186.
24. LLOPART, A., S. ELWYN, D. LACHAISE and J. A. COYNE, 2002 Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea. Evolution 56: 2262-2277.
25. MCDONALD, J. H., and M. KREITMAN, 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654.
26. NIELSEN, R., and Z. YANG, 1998 Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929-936.
27. PATTEN, M. M., and D. HAIG, 2009 Maintenance or loss of genetic variation under sexual and parental antagonism at a sex-linked locus. Evolution 63: 2888-2895.
28. PETROV, D. A., E. R. LOZOVSKAYA and D. L. HARTL, 1996 High intrinsic rate of DNA loss in Drosophila. Nature 384: 346-349.
29. POND, S. L., and S. D. FROST, 2005 Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531-2533.
30. POWELL, J. R., 1997 Progress and Prospects in Evolutionary Biology: The Drosophila Model. Oxford University Press, New York.
31. PRESGRAVES, D. C., 2007 Does genetic conflict drive rapid molecular evolution of nuclear transport genes in Drosophila? Bioessays 29: 386-391.
32. PRESGRAVES, D. C., and W. STEPHAN, 2007 Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96. Mol. Biol. Evol. 24: 306-314.
33. PROULX, S. R., and P. C. PHILLIPS, 2006 Allelic divergence precedes and promotes gene duplication. Evolution 60: 881-892.
34. QUIMBY, B. B., T. LAMITINA, S. W. L'HERNAULT and A. H. CORBETT, 2000 The mechanism of ran import into the nucleus by nuclear transport factor 2. J. Biol. Chem. 275: 28575-28582.
35. RANZ, J. M., C. I. CASTILLO-DAVIS, C. D. MEIKLEJOHN and D. L. HARTL, 2003 Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300: 1742-1745.
36. RIBBECK, K., G. LIPOWSKY, H. M. KENT, M. STEWART and D. GORLICH, 1998 NTF2 mediates nuclear import of Ran. EMBO J. 17: 6587-6598.
37. RICE, W. R., 1984 Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735-742. (Pubitemid 16277746)
38. SCHLENKE, T. A., and D. J. BEGUN, 2003 Natural selection drives Drosophila immune system evolution. Genetics 164: 1471-1480.
39. SCHMITTGEN, T. D., and K. J. LIVAK, 2008 Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101-1108.
40. SLATKIN, M., and B. RANNALA, 2000 Estimating allele age. Annu. Rev. Genomics Hum. Genet. 1: 225-249.
41. TAJIMA, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
42. THOMPSON, J. D., D. G. HIGGINS and T. J. GIBSON, 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
43. TURNER, J. M., 2007 Meiotic sex chromosome inactivation. Development 134: 1823-1831.
44. TURNER, J. M., S. K. MAHADEVAIAH, O. FERNANDEZ-CAPETILLO, A. NUSSENZWEIG, X. XU et al., 2005 Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 37: 41-47.
45. VICOSO, B., and B. CHARLESWORTH, 2009 The deficit of male-biased genes on the D. melanogaster X chromosome is expression-dependent: A consequence of dosage compensation? J. Mol. Evol. 68: 576-583.
46. WATTERSON, G. A., 1975 On the number of segragating sites in genetical models without recombination. Theor. Popul. Biol. 7: 256-276.
47. YANG, Z., 1998 Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15: 568-573.
48. YANG, Z., 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591.
49. YANG, Z., R. NIELSEN, N. GOLDMAN and A. M. PEDERSEN, 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
50. ZHANG, Y., D. STURGILL, M. PARISI, S. KUMAR and B. OLIVER, 2007 Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450: 233-237.