Parallel faster-X evolution of gene expression and protein sequences in Drosophila: Beyond differences in expression properties and protein interactions

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Llopart, Ana ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; AUTOSOME; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA SANTOMEA; DROSOPHILA YAKUBA; GENDER BIAS; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HEMIZYGOSITY; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN INTERACTION; TISSUE SPECIFICITY; X CHROMOSOME; ANIMAL; ANTIBODY SPECIFICITY; DNA SEQUENCE; GENETICS; INSECT CHROMOSOME; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; X CHROMOSOMAL INHERITANCE;

DROSOPHILA SANTOMEA; DROSOPHILA YAKUBA;

DROSOPHILA PROTEIN;

ANIMALS; BASE SEQUENCE; CHROMOSOMES, INSECT; DROSOPHILA; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, X-LINKED; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; SEQUENCE ANALYSIS, DNA; X CHROMOSOME;

EID: 84925867850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116829     Document Type: Article

References (96)

1. Charlesworth B, Coyne JA, Barton N (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113-146.
2. Vicoso B, Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7: 645-653. PMID: 16847464
3. Herrig DK, Llopart A (2014) Evolution of X-linked male-baised genes in Drosophila. In: Encyclopedia of Life Sciences: John Wiley & Sons, Ltd: Chichester. doi: 10.1002/9780470015902.a0025537.
4. Vicoso B, Charlesworth B (2009) Effective population size and the faster-X effect: an extended model. Evolution 63: 2413-2426. doi: 10.1111/j.1558-5646.2009.00719.x PMID: 19473388
5. Mank JE, Vicoso B, Berlin S, Charlesworth B (2010) Effective population size and the Faster-X effect: empirical results and their interpretation. Evolution 64: 663-674. doi: 10.1111/j.1558-5646.2009.00853.x PMID: 19796145
6. Mank JE, Nam K, Ellegren H (2010) Faster-Z evolution is predominantly due to genetic drift. Mol Biol Evol 27: 661-670. doi: 10.1093/molbev/msp282 PMID: 19926635
7. Mank JE, Axelsson E, Ellegren H (2007) Fast-X on the Z: rapid evolution of sex-linked genes in birds. Genome Res 17: 618-624. PMID: 17416747
8. Ellegren H (2009) Genomic evidence for a large-Z effect. Proc Biol Sci 276: 361-366. doi: 10.1098/rspb.2008.1135 PMID: 18826931
9. Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52: 223-235. PMID: 2854088
10. Charlesworth B (2012) The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome. Genetics 191: 233-246. doi: 10. 1534/genetics.111.138073 PMID: 22377629
11. Vicoso B, Charlesworth B (2009) Recombination rates may affect the ratio of X to autosomal noncoding polymorphism in African populations of Drosophila melanogaster. Genetics 181: 1699-1701. doi: 10.1534/genetics.108.098004 PMID: 19189953
12. Charlesworth B (2001) The effect of life-history and mode of inheritance on neutral genetic variability. Genet Res 77: 153-166. PMID: 11355571
13. Comeron JM (2014) Background Selection as Baseline for Nucleotide Variation across the Drosophila Genome. PLoS Genet 10: e1004434. doi: 10.1371/journal.pgen.1004434 PMID: 24968283
14. Thornton K, Long M (2002) Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol Biol Evol 19: 918-925. PMID: 12032248
15. Thornton K, Long M (2005) Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster. Mol Biol Evol 22: 273-284. PMID: 15483321
16. Betancourt AJ, Presgraves DC, Swanson WJ (2002) A Test for Faster X Evolution in Drosophila. Mol Biol Evol 19: 1816-1819. PMID: 12270910
17. Thornton K, Bachtrog D, Andolfatto P (2006) X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution. Genome Res 16: 498-504. PMID: 16520459
18. Counterman BA, Ortiz-Barrientos D, Noor MA (2004) Using comparative genomic data to test for fast-X evolution. Evolution 58: 656-660. PMID: 15119449
19. Connallon T (2007) Adaptive protein evolution of X-linked and autosomal genes in Drosophila: implications for faster-X hypotheses. Mol Biol Evol 24: 2566-2572. PMID: 17884828
20. Grath S, Parsch J (2012) Rate of amino acid substitution is influenced by the degree and conservation of male-biased transcription over 50 million years of Drosophila evolution. Genome Biol Evol 4: 346-359. doi: 10.1093/gbe/evs012 PMID: 22321769
21. Campos JL, Halligan DL, Haddrill PR, Charlesworth B (2014) The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster. Mol Biol Evol 31: 1010-1028. doi: 10.1093/molbev/msu056 PMID: 24489114
22. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, et al. (2007) Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310. PMID: 17988176
23. Musters H, Huntley MA, Singh RS (2006) A genomic comparison of faster-sex, faster-X, and fastermale evolution between Drosophila melanogaster and Drosophila pseudoobscura. J Mol Evol 62: 693-700. PMID: 16612543
24. Hu TT, Eisen MB, Thornton KR, Andolfatto P (2013) A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res 23: 89-98. doi: 10.1101/gr.141689.112 PMID: 22936249
25. Vicoso B, Haddrill PR, Charlesworth B (2008) A multispecies approach for comparing sequence evolution of X-linked and autosomal sites in Drosophila. Genet Res (Camb) 90: 421-431. doi: 10.1017/S0016672308009804 PMID: 19061532
26. Baines JF, Sawyer SA, Hartl DL, Parsch J (2008) Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila. Mol Biol Evol 25: 1639-1650. doi: 10.1093/molbev/msn111 PMID: 18477586
27. Bachtrog D, Jensen JD, Zhang Z (2009) Accelerated adaptive evolution on a newly formed X chromosome. PLoS Biol 7: e82. doi: 10.1371/journal.pbio.1000082 PMID: 19402745
28. Singh ND, Larracuente AM, Clark AG (2008) Contrasting the efficacy of selection on the X and autosomes in Drosophila. Mol Biol Evol 25: 454-467. PMID: 18083702
29. Muller L, Grath S, von Heckel K, Parsch J (2012) Inter- and intraspecific variation in Drosophila genes with sex-biased expression. Int J Evol Biol 2012: 963976. doi: 10.1155/2012/963976 PMID: 22315698
30. Garrigan D, Kingan SB, Geneva AJ, Vedanayagam JP, Presgraves DC (2014) Genome Diversity and Divergence in Drosophila mauritiana: Multiple Signatures of Faster X Evolution. Genome Biol Evol 6: 2444-2458. doi: 10.1093/gbe/evu198 PMID: 25193308
31. Langley CH, Stevens K, Cardeno C, Lee YC, Schrider DR, et al. (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533-598. doi: 10.1534/genetics.112.142018 PMID: 22673804
32. Lu J, Wu CI (2005) Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci U S A 102: 4063-4067. PMID: 15728731
33. Veeramah KR, Gutenkunst RN, Woerner AE, Watkins JC, Hammer MF (2014) Evidence for increased levels of positive and negative selection on the X chromosome versus autosomes in humans. Mol Biol Evol.
34. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, et al. (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3: e170. PMID: 15869325
35. Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M, et al. (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309: 1850-1854. PMID: 16141373
36. Hvilsom C, Qian Y, Bataillon T, Li Y, Mailund T, et al. (2012) Extensive X-linked adaptive evolution in central chimpanzees. Proc Natl Acad Sci U S A 109: 2054-2059. doi: 10.1073/pnas.1106877109 PMID: 22308321
37. Baines JF, Harr B (2007) Reduced X-linked diversity in derived populations of house mice. Genetics 175: 1911-1921. PMID: 17287527
38. Kousathanas A, Halligan DL, Keightley PD (2014) Faster-X adaptive protein evolution in house mice. Genetics 196: 1131-1143. doi: 10.1534/genetics.113.158246 PMID: 24361937
39. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11: e1001643. doi: 10.1371/journal.pbio.1001643 PMID: 24015111
40. Jovelin R (2013) Pleiotropic constraints, expression level, and the evolution of miRNA sequences. J Mol Evol 77: 206-220. doi: 10.1007/s00239-013-9588-6 PMID: 24100521
41. Sackton TB, Corbett-Detig RB, Nagaraju J, Vaishna L, Arunkumar KP, et al. (2014) Positive Selection Drives Faster-Z Evolution in Silkmoths. Evolution.
42. Jaquiery J, Stoeckel S, Rispe C, Mieuzet L, Legeai F, et al. (2012) Accelerated evolution of sex chromosomes in aphids, an x0 system. Mol Biol Evol 29: 837-847. doi: 10.1093/molbev/msr252 PMID: 21998277
43. Llopart A (2012) The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea and their hybrids. Mol Biol Evol 29: 3873-3886. doi: 10.1093/molbev/mss190 PMID: 22844069
44. Kayserili MA, Gerrard DT, Tomancak P, Kalinka AT (2012) An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis. PLoS Genet 8: e1003200. doi: 10.1371/journal.pgen.1003200 PMID: 23300473
45. Meisel RP, Malone JH, Clark AG (2012) Faster-X evolution of gene expression in Drosophila. PLoS Genet 8: e1003013. doi: 10.1371/journal.pgen.1003013 PMID: 23071459
46. Meisel RP (2011) Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Mol Biol Evol 28: 1893-1900. doi: 10.1093/molbev/msr010 PMID: 21239389
47. Meisel RP, Malone JH, Clark AG (2012) Disentangling the relationship between sex-biased gene expression and X-linkage. Genome Res 22: 1255-1265. doi: 10.1101/gr.132100.111 PMID: 22499666
48. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, et al. (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697-700. PMID: 12511656
49. Sturgill D, Zhang Y, Parisi M, Oliver B (2007) Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 238-241. PMID: 17994090
50. Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B (2007) Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450: 233-237. PMID: 17994089
51. Meiklejohn CD, Presgraves DC (2012) Little evidence for demasculinization of the Drosophila X chromosome among genes expressed in the male germline. Genome Biol Evol 4: 1007-1016. doi: 10.1093/gbe/evs077 PMID: 22975718
52. Meiklejohn CD, Landeen EL, Cook JM, Kingan SB, Presgraves DC (2011) Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation. PLoS Biol 9: e1001126. doi: 10.1371/journal.pbio.1001126 PMID: 21857805
53. Mikhaylova LM, Nurminsky DI (2011) Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome. BMC Biol 9: 29. doi: 10.1186/1741-7007-9-29 PMID: 21542906
54. Vibranovski MD, Lopes HF, Karr TL, Long M (2009) Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet 5: e1000731. doi: 10.1371/journal.pgen.1000731 PMID: 19936020
55. Chang PL, Dunham JP, Nuzhdin SV, Arbeitman MN (2011) Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics 12: 364. doi: 10. 1186/1471-2164-12-364 PMID: 21756339
56. Catalan A, Hutter S, Parsch J (2012) Population and sex differences in Drosophila melanogaster brain gene expression. BMC Genomics 13: 654. doi: 10.1186/1471-2164-13-654 PMID: 23170910
57. Marbach D, Roy S, Ay F, Meyer PE, Candeias R, et al. (2012) Predictive regulatory models in Drosophila melanogaster by integrative inference of transcriptional networks. Genome Res 22: 1334-1349. doi: 10.1101/gr.127191.111 PMID: 22456606
58. Hansen ME, Kulathinal RJ (2013) Sex-biased networks and nodes of sexually antagonistic conflict in Drosophila. Int J Evol Biol 2013: 545392. doi: 10.1155/2013/545392 PMID: 23431497
59. Larracuente AM, Sackton TB, Greenberg AJ, Wong A, Singh ND, et al. (2008) Evolution of proteincoding genes in Drosophila. Trends Genet 24: 114-123. doi: 10.1016/j.tig.2007.12.001 PMID: 18249460
60. Marais G, Domazet-Loso T, Tautz D, Charlesworth B (2004) Correlated evolution of synonymous and nonsynonymous sites in Drosophila. J Mol Evol 59: 771-779. PMID: 15599509
61. Nuzhdin SV, Wayne ML, Harmon KL, McIntyre LM (2004) Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol 21: 1308-1317. PMID: 15034135
62. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH (2005) Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 102: 14338-14343. PMID: 16176987
63. Pal C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158: 927-931. PMID: 11430355
64. Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL (2005) Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Mol Biol Evol 22: 1345-1354. PMID: 15746013
65. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW (2002) Evolutionary rate in the protein interaction network. Science 296: 750-752. PMID: 11976460
66. Cariou ML, Silvain JF, Daubin V, Da Lage JL, Lachaise D (2001) Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line. Molecular Ecology 10: 649-660. PMID: 11298976
67. Llopart A, Lachaise D, Coyne JA (2005) Multilocus analysis of introgression between two sympatric sister species of Drosophila : Drosophila yakuba and D. santomea. Genetics 171: 197-210. PMID: 15965264
68. Llopart A, Lachaise D, Coyne JA (2005) An anomalous hybrid zone in Drosophila. Evolution 59: 2602-2607. PMID: 16526507
69. Ashburner M (1989) Drosophila: A Laboratory Manual. Cold Spring Harbor, NY.: Cold Spring Harbor Laboratory Press.
70. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079. doi: 10.1093/bioinformatics/btp352 PMID: 19505943
71. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218. PMID: 17994087
72. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760. doi: 10.1093/bioinformatics/btp324 PMID: 19451168
73. Blankenberg D, Kuster GV, Coraor N, Ananda G, Lazarus R, et al. (2001) Galaxy: A Web-Based Genome Analysis Tool for Experimentalists. Current Protocols in Molecular Biology: John Wiley & Sons, Inc. doi: 10.1002/0471142700.nca01bs00 PMID: 18428806
74. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, et al. (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15: 1451-1455. PMID: 16169926
75. Goecks J, Nekrutenko A, Taylor J (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86. doi: 10.1186/gb-2010-11-8-r86 PMID: 20738864
76. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, et al. (2005) Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21: 650-659. PMID: 15388519
77. Chintapalli VR, Wang J, Dow JA (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720. PMID: 17534367
78. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in Biosciences 13: 555-556. PMID: 9367129
79. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586-1591. PMID: 17483113
80. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favorable gene. Genetical Research 23: 23-35. PMID: 4407212
81. Gillespie JH (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155: 909-919. PMID: 10835409
82. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L, et al. (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10: e1001388. doi: 10.1371/journal.pbio.1001388 PMID: 22984349
83. Campos JL, Zeng K, Parker DJ, Charlesworth B, Haddrill PR (2013) Codon usage bias and effective population sizes on the X chromosome versus the autosomes in Drosophila melanogaster. Mol Biol Evol 30: 811-823. doi: 10.1093/molbev/mss222 PMID: 23204387
84. Singh ND, Davis JC, Petrov DA (2005) Codon bias and noncoding GC content correlate negatively with recombination rate on the Drosophila X chromosome. J Mol Evol 61: 315-324. PMID: 16044248
85. Singh ND, Davis JC, Petrov DA (2005) X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis. Genetics 171: 145-155. PMID: 15965246
86. Vicario S, Moriyama EN, Powell JR (2007) Codon usage in twelve species of Drosophila. BMC Evol Biol 7: 226. PMID: 18005411
87. Begun DJ, Whitley P, Todd BL, Waldrip-Dail HM, Clark AG (2000) Molecular population genetics of male accessory gland proteins in Drosophila. Genetics 156: 1879-1888. PMID: 11102381
88. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, et al. (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177: 1321-1335. PMID: 18039869
89. Jiang ZF, Machado CA (2009) Evolution of sex-dependent gene expression in three recently diverged species of Drosophila. Genetics 183: 1175-1185. doi: 10.1534/genetics.109.105775 PMID: 19720861
90. Zhang Z, Hambuch TM, Parsch J (2004) Molecular evolution of sex-biased genes in Drosophila. Mol Biol Evol 21: 2130-2139. PMID: 15282334
91. Proschel M, Zhang Z, Parsch J (2006) Widespread adaptive evolution of Drosophila genes with sexbiased expression. Genetics 174: 893-900. PMID: 16951084
92. Perry JC, Harrison PW, Mank JE (2014) The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster. Mol Biol Evol 31: 1206-1219. doi: 10.1093/molbev/msu072 PMID: 24526011
93. Wu C-I, Davis AW (1993) Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases. Am Nat 142: 187-212. doi: 10.1086/285534 PMID: 19425975
94. Wu CI, Johnson N, Palopoli MF (1996) Haldane's rule and its legacy: why are there so many sterile males. Trends Ecol Evol 11: 281-284. PMID: 21237844
95. Begun DJ, Whitley P (2000) Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci USA 97: 5960-5965. PMID: 10823947
96. Comeron JM, Ratnappan R, Bailin S (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genetics 8: e1002905. doi: 10.1371/journal.pgen.1002905 PMID: 23071443