Sex chromosomes and the evolution of sexual dimorphism: Lessons from the genome

American Naturalist

Volumn 173, Issue 2, 2009, Pages 141-150

  Mank, Judith E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Evolutionary genomics; Sex biased gene expression; Sexual antagonism; X chromosome; Z chromosome

Indexed keywords

ANTAGONISM; CHROMOSOME; EVOLUTIONARY BIOLOGY; GAMETE; GENE EXPRESSION; SEXUAL DIMORPHISM;

ANIMAL; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GENOME; MALE; PHENOTYPE; REVIEW; SEX CHROMOSOME; SEXUAL DEVELOPMENT;

ANIMALS; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENOME; MALE; PHENOTYPE; SEX CHARACTERISTICS; SEX CHROMOSOMES; BIOLOGICAL EVOLUTION;

ANIMALIA;

EID: 61849152920     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/595754     Document Type: Review

References (78)

1. Albert, A. Y. K., and S. P. Otto. 2005. Sexual selection can resolve sex-linked sexual antagonism. Science 310:119-121.
2. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
3. Baines, J. F., S. A. Sawyer, D. L. Hartl, and J. Parsch. 2008. Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila. Molecular Biology and Evolution 25:1639-1650.
4. Charlesworth, B., J. A. Coyne, and N. H. Barton. 1987. The relative rates of evolution of sex chromosomes and autosomes. American Naturalist 130:113-146.
5. Chenoweth, S. F., H. D. Rundle, and M. W. Blows. 2008. Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection. American Naturalist 171:22-34.
6. Chippindale, A. K., J. R. Gibson, and W. R. Rice. 2001. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proceedings of the National Academy of Sciences of the USA 98:1671-1675.
7. Clotfelter, E. D., D. M. O'Neal, J. M. Gaudioso, J. M. Casto, I. M. Parker-Renga, E. A. Snajdr, D. L. Duffy, et al. 2004. Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Hormones and Behavior 46:171-178.
8. Connallon, T. 2007. Adaptive protein evolution of X-linked and autosomal genes in Drosophila: implications for faster-X hypotheses. Molecular Biology and Evolution 24:2566-2572.
9. Connallon, T., and L. L. Knowles. 2005. Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends in Genetics 21:495-499.
10. Counterman, B. A., D. Ortiz-Barrientos, and M. A. F. Noor. 2004. Using comparative genomic data to test for fast-X evolution. Evolution 58:656-660.
11. Coyne, J. A., E. H. Kay, and S. Pruett-Jones. 2008. The genetic basis of sexual dimorphism in birds. Evolution 62:214-219.
12. Cutter, A. D., and S. Ward. 2005. Sexual and temporal dynamics of molecular evolution in C. elegans development. Molecular Biology and Evolution 22:178-188.
13. Day, T., and R. Bonduriansky. 2004. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167:1537-1546.
14. Ducrest, A.-L., L. Keller, and A. Roulin. 2008. Pleiotropy in the melanocortin system, coloration and behavioral syndromes. Trends in Ecology & Evolution 23:502-510.
15. Ellegren, H., L. Hultin-Rosenberg, B. Brunström, L. Dencker, K. Kultima, and B. Scholtz. 2007. Faced with inequality: chicken does not have general dosage compensation of sex-linked genes. BMC Biology 5:40.
16. Enstrom, D. A., E. D. Ketterson, and V. Nolan. 1997. Testosterone and mate choice in the dark-eyed junco. Animal Behaviour 54: 1135-1146.
17. Fairbairn, D. J., and D. A. Roff. 2006. The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage. Heredity 97:319-328.
18. Fitzpatrick, M. J. 2004. Pleiotropy and the genomic location of sexually selected genes. American Naturalist 163:800-808.
19. Gleason, J. M., S. V. Nuzhdin, and M. G. Ritchie. 2002. Quantitative trait loci affecting a courtship signal in Drosophila melanogaster. Heredity 89:1-6.
20. Good, J. M., and M. W. Nachman. 2005. Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Molecular Biology and Evolution 22:1044-1052.
21. Gupta, V., M. Parisi, D. Sturgill, R. Nuttall, M. Doctolero, O. K. Dudko, J. D. Malley, et al. 2006. Global analysis of X-chromosome dosage compensation. Journal of Biology 5:3.
22. Hense, W., J. F. Baines, and J. Parsch. 2007. X chromosome inactivation during Drosophila spermatogenesis. PLoS Biology 5:2288-2295.
23. Hill, J. A., D. A. Enstrom, E. D. Ketterson, V. Nolan, and C. Ziegenfus. 1999. Mate choice based on static versus dynamic secondary sexual traits in the dark-eyed junco. Behavioral Ecology 10:91-96.
24. Itoh, Y., E. Melamed, X. Yang, K. Kampf, S. Wang, N. Yehya, A. van Nas, et al. 2007. Dosage compensation is less effective in birds than in mammals. Journal of Biology 6:2.
25. Iyengar, V. K., H. K. Reeve, and T. Eisner. 2002. Paternal inheritance of a female moth's mating preference. Nature 419:830-832.
26. Johnston, C. M., F. L. Lovell, D. A. Leongamornlert, B. E. Stranger, E. T. Dermitzakis, and M. T. Ross. 2008. Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genetics 4:e9.
27. Judson, O. 2002. Dr. Tatiana's sex advice to all creation: the definitive guide to the evolution of sex. Metropolitan Books, New York.
28. Kaiser, V. B., and H. Ellegren. 2006. Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60: 1945-1951.
29. Ketterson, E. D., V. Nolan, and M. Sandell. 2005. Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? American Naturalist 166(suppl.):S85-S98.
30. Khaitovich, P., I. Hellmann, W. Enard, K. Nowick, M. Leinweber, H. Franz, G. Weiss, et al. 2005. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850-1854.
31. Khil, P. P., N. A. Smirnova, P. J. Romanienko, and R. D. Camerini-Otero. 2004. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nature Genetics 36:642-646.
32. Kirkpatrick, M., and D. W. Hall. 2004. Sexual selection and sex linkage. Evolution 58:683-691.
33. Kopp, A., I. Duncan, and S. B. Carroll. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:553-559.
34. Lin, H., V. Gupta, M. D. VerMilyea, F. Faliani, J. T. Lee, L. P. O'Neill, and B. M. Turner. 2007. Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biology 5:e326.
35. Lindholm, A., and F. Breden. 2002. Sex chromosomes and sexual selection in poeciliid fishes. American Naturalist 160(suppl.):S214-S224.
36. Lucchesi, J. C., W. G. Kelly, and B. Parming. 2005. Chromatin remodeling in dosage compensation. Annual Review of Genetics 39: 615-651.
37. Lyon, M. F. 1999. X-chromosome inactivation. Current Biology 9: R235-R237.
38. Mank, J. E. 2007a. The evolution of sexually selected traits and an tagonistic androgen expression in actinopterygiian fishes. American Naturalist 169:142-149.
39. -. 2007b. Mating preferences, sexual selection, and patterns of cladogenesis in ray-finned fishes. Journal of Evolutionary Biology 20:597-602.
40. Mank, J. E., and H. Ellegren. Forthcoming. Sex linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Nature.
41. Mank, J. E., D. E. L. Promislow, and J. C. Avise. 2005. Phylogenetic perspectives on the evolution of parental care in ray-finned fishes. Evolution 59:1570-1578.
42. -. 2006a. Evolution of alternative sex determining mechanisms in teleost fishes. Biological Journal of the Linnean Society 87:83-93.
43. Mank, J. E., D. W. Hall, M. Kirkpatrick, and J. C. Avise. 2006b. Sex chromosomes and male ornaments: a comparative evaluation in ray-finned fishes. Proceedings of the Royal Society B: Biological Sciences 273:233-236.
44. Mank, J. E., E. Axelsson, and H. Ellegren. 2007a. Fast-X on the Z: rapid evolution of sex-linked genes in birds. Genome Research 17: 618-624.
45. Mank, J. E., L. Hultin-Rosenberg, E. Axelsson, and H. Ellegren. 2007b. Rapid evolution of female-biased, but not male-biased, genes expressed in avian brain. Molecular Biology and Evolution 24:2698-2706.
46. Mank, J. E., L. Hultin-Rosenberg, M. Zwahlen, and H. Ellegren. 2008a. Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. American Naturalist 171: 35-43.
47. Mank, J. E., L. Hultin-Rosenberg, M. T. Webster, and H. Ellegren. 2008b. The unique genomic properties of sex-biased genes: insights from avian microarray data. BMC Genomics 9:148.
48. Meiklejohn, C. D., J. Parsch, J. M. Ranz, and D. L. Hartl. 2003. Rapid evolution of male-biased gene expression in Drosophila. Proceedings of the National Academy of Sciences of the USA 100:9894-9899.
49. Meyer, B. J., and L. P. Casson. 1986. Caenorhabditis elegans compensates for the difference in X-chromosome dosage between the sexes by regulating transcript levels. Cell 47:871-881.
50. Meyer, B. J., P. McDonel, G. Csankovszki, and E. Ralston. 2004. Sex and X-chromosome-wide repression in Caenorhabditis elegans. Cold Spring Harbor Symposia on Quantitative Biology 69:71-79.
51. Mikkelsen, T. S., M. C. Ku, D. B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560.
52. Morison, I. M., J. P. Ramsay, and H. G. Spencer. 2005. A census of mammalian imprinting. Trends in Genetics 21:457-465.
53. Mueller, J. L., S. K. Mahadevaiah, P. J. Park, P. R. Warburton, D. C. Page, and J. M. A. Turner. 2008. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nature Genetics 40:794-799.
54. Namekawa, S. H., P. J. Park, L. F. Zhang, J. E. Shima, J. R. McCarrey, M. D. Griswold, and J. T. Lee. 2006. Postmeiotic sex chromatin in the male germline of mice. Current Biology 16:660-667.
55. Nguyen, D. K., and C. M. Disteche. 2006. Dosage compensation of the active X chromosome in mammals. Nature Genetics 38:47-53.
56. Parisi, M., R. Nuttall, D. Naiman, G. Bouffard, J. Malley, J. Andrews, S. Eastman, et al. 2003. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299:697-700.
57. Parisi, M., R. Nuttall, P. Edwards, J. Minor, D. Naiman, J. N. Lu, M. Doctolero, et al. 2004. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biology 5:R40.
58. Parker, G. A., R. R. Baker, and V. G. F. Smith. 1972. The origin and evolution of gamete dimorphism and the male-female phenomenon. Journal of Theoretical Biology 36:529-553.
59. Poissant, J., A. J. Wilson, M. Festa-Bianchet, J. T. Hogg, and D. W. Coltman. 2008. Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep. Proceedings of the Royal Society B: Biological Sciences 275:623-628.
60. Potrzebowski, L., N. Vinckenbosch, A. C. Marques, F. Chalmel, B. Jegou, and H. Kaessmann. 2008. Chromosomal gene movements reflect the recent origin and biology of the therian sex chromosomes. PLoS Biology 6:e80.
61. Pröschel, M., Z. Zhang, and J. Parsch. 2005. Widespread adaptive evolution of Drosophila genes with sex-biased expression. Genetics 174:893-900.
62. 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.
63. Reeve, H. K., and D. W. Pfennig. 2003. Genetic biases for showy males: are some genetic systems especially conducive to sexual selection? Proceedings of the National Academy of Sciences of the USA 100:1089-1094.
64. Reinhold, K. 1998. Sex linkage among genes controlling sexually selected traits. Behavioral Ecology and Sociobiology 44:1-7.
65. Reinius, B., P. Saetre, J. A. Leonard, R. Blekhman, R. Merino-Martinez, Y. Gilad, and E. Jazin. 2008. An evolutionarily conserved sexual signature in the primate brain. PLoS Genetics 4:e1000100.
66. Rice, W. R. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735-742.
67. Ritchie, M. G. 2000. The inheritance of female preference functions in a mate recognition system. Proceedings of the Royal Society B: Biological Sciences 267:327-332.
68. Saether, S. A., G. P. Saetre, T. Borge, C. Wiley, N. Svedin, G. Andersson, T. Veen, et al. 2007. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318:95-97.
69. Storchova, R., and P. Divina. 2006. Nonrandom representation of sex-biased genes on chicken Z chromosome. Journal of Molecular Evolution 63:676-681.
70. Sturgill, D., Y. Zhang, M. Parisi, and B. Oliver. 2007. Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 233-237.
71. Turner, J. M. A. 2007. Meiotic sex chromosome inactivation. Development 134:1823-1831.
72. Turner, L. M., E. B. Chuong, and H. E. Hoekstra. 2008. Comparative analysis of testis protein evolution in rodents. Genetics 179:2075-2089.
73. Vicoso, B., and B. Charlesworth. 2006. Evolution on the X chromosome: unusual patterns and processes. Nature Reviews Genetics 7:645-653.
74. Wolfenbarger, L. L., and G. S.Wilkinson. 2001. Sex-linked expression of a sexually selected trait in the stalk-eyed fly, Cyrtodiopsis dalmanni. Evolution 55:103-110.
75. Yang, X., E. E. Schadt, S. Wang, H. Wang, A. P. Arnold, L. Ingram-Drake, T. A. Drake, et al. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Research 16:995-1004.
76. Zauner, H., G. Begemann, M. Mari-Beffa, and A. Meyer. 2003. Differential regulation of msx genes in the development of the gonopodium, an intromittent organ, and of the "sword," a sexually selected trait of swordtail fishes (Xiphophorus). Evolution and Development 5:466-477.
77. 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 450:233-238.
78. Zhang, Z., T. M. Hambuch, and J. Parsch. 2004. Molecular evolution of sex-biased genes in Drosophila. Molecular Biology and Evolution 21:2130-2139.