Sex-Differential Selection and the Evolution of X Inactivation Strategies
X inactivation—the transcriptional silencing of one X chromosome copy per female somatic cell—is universal among therian mammals, yet the choice of which X to silence exhibits considerable variation among species. X inactivation strategies can range from strict paternally inherited X inactivation (PXI), which renders females haploid for all maternally inherited alleles, to unbiased random X inactivation (RXI), which equalizes expression of maternally and paternally inherited alleles in each female tissue. However, the underlying evolutionary processes that might account for this observed diversity of X inactivation strategies remain unclear. We present a theoretical population genetic analysis of X inactivation evolution and specifically consider how conditions of dominance, linkage, recombination, and sex-differential selection each influence evolutionary trajectories of X inactivation. The results indicate that a single, critical interaction between allelic dominance and sex-differential selection can select for a broad and continuous range of X inactivation strategies, including unequal rates of inactivation between maternally and paternally inherited X chromosomes. RXI is favored over complete PXI as long as alleles deleterious to female fitness are sufficiently recessive, and the criteria for RXI evolution is considerably more restrictive when fitness variation is sexually antagonistic (i.e., alleles deleterious to females are beneficial to males) relative to variation that is deleterious to both sexes. Evolutionary transitions from PXI to RXI also generally increase mean relative female fitness at the expense of decreased male fitness. These results provide a theoretical framework for predicting and interpreting the evolution of chromosome-wide expression of X-linked genes and lead to several useful predictions that could motivate future studies of allele-specific gene expression variation.
Vyšlo v časopise:
Sex-Differential Selection and the Evolution of X Inactivation Strategies. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003440
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003440
Souhrn
X inactivation—the transcriptional silencing of one X chromosome copy per female somatic cell—is universal among therian mammals, yet the choice of which X to silence exhibits considerable variation among species. X inactivation strategies can range from strict paternally inherited X inactivation (PXI), which renders females haploid for all maternally inherited alleles, to unbiased random X inactivation (RXI), which equalizes expression of maternally and paternally inherited alleles in each female tissue. However, the underlying evolutionary processes that might account for this observed diversity of X inactivation strategies remain unclear. We present a theoretical population genetic analysis of X inactivation evolution and specifically consider how conditions of dominance, linkage, recombination, and sex-differential selection each influence evolutionary trajectories of X inactivation. The results indicate that a single, critical interaction between allelic dominance and sex-differential selection can select for a broad and continuous range of X inactivation strategies, including unequal rates of inactivation between maternally and paternally inherited X chromosomes. RXI is favored over complete PXI as long as alleles deleterious to female fitness are sufficiently recessive, and the criteria for RXI evolution is considerably more restrictive when fitness variation is sexually antagonistic (i.e., alleles deleterious to females are beneficial to males) relative to variation that is deleterious to both sexes. Evolutionary transitions from PXI to RXI also generally increase mean relative female fitness at the expense of decreased male fitness. These results provide a theoretical framework for predicting and interpreting the evolution of chromosome-wide expression of X-linked genes and lead to several useful predictions that could motivate future studies of allele-specific gene expression variation.
Zdroje
1. PayerB, LeeJT (2008) X chromosome dosage compensation: how mammals keep the balance. Ann Rev Genet 42: 733–772.
2. DeakinJE, ChaumeilJ, HoreTA, GravesJAM (2009) Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Research 17: 671–685.
3. CooperDW, VandeBergJL, SharmanGB, PooleWE (1971) Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nature New Biology 230: 155–157.
4. SharmanGB (1971) Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230: 231–232.
5. LyonMF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372–373.
6. WangX, SolowayPD, ClarkAG (2010) Paternally biased X inactivation in mouse neonatal brain. Genome Biology 11: R79.
7. GreggC, ZhangJ, ButlerJE, HaigD, DulacC (2010) Sex-specific parent-of-origin allelic expression in the mouse brain. Science 329: 682–685.
8. CooperDW, JohnstonPG, GravesJAM (1993) X-inactivation in marsupials and monotremes. Seminars in Developmental Biology 4: 117–128.
9. ChandraHS, BrownSW (1975) Chromosome imprinting and the mammalian X chromosome. Nature 253: 165–168.
10. CharlesworthB (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75: 5618–5622.
11. CharlesworthB (1996) The evolution of chromosomal sex determination and dosage compensation. Current Biology 6: 149–162.
12. SimmonsMJ, CrowJF (1977) Mutations affecting fitness in Drosophila populations. Ann Rev Genet 11: 49–78.
13. CharlesworthB, CharlesworthD (1999) The genetic basis of inbreeding depression. Genet Res 74: 329–340.
14. Charlesworth B, Hughes KA (1999) The maintenance of genetic variation in life-history traits. Pp. 369–392 in RS Singh and CB Krimbas, eds. Evolutionary genetics: from molecules to morphology, vol. 1 Cambridge University Press, Cambridge, UK.
15. HalliganDL, KeightleyPD (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evol Syst 40: 151–172.
16. LyonMF (1988) The William Allan Memorial Award Address: X-chromosome inactivation and the location and expression of X-linked genes. Am J Hum Genet 42: 8–16.
17. MooreT, HaigD (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends in Genetics 7: 45–49.
18. HaigD (2006) Self-imposed silence: parental antagonism and the evolution of X-chromosome inactivation. Evolution 60: 440–447.
19. EngelstädterJ, HaigD (2008) Sexual antagonism and the evolution of X chromosome inactivation. Evolution 62: 2097–2104.
20. MankJE (2009) The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet 25: 226–233.
21. CrowJF, KimuraM (1965) Evolution in sexual and asexual populations. Am Nat 99: 439–450.
22. CharlesworthB (1991) When to be diploid. Nature 351: 273–274.
23. KondrashovAS, CrowJF (1991) Haploidy or diploidy: which is better? Nature 351: 314–315.
24. PerrotV, RicherdS, ValéroM (1991) Transition from haploidy to diploidy. Nature 351: 315–317.
25. OttoSP, GersteinAC (2008) The evolution of haploidy and diploidy. Current Biology 18: R1121–R1124.
26. OttoSP, GoldsteinDB (1992) Recombination and the evolution of diploidy. Genetics 131: 745–751.
27. BengtssonBO (1992) Deleterious mutations and the origin of the meiotic ploidy cycle. Genetics 131: 741–744.
28. JenkinsCD, KirkpatrickM (1995) Deleterious mutation and the evolution of genetic life cycles. Evolution 49: 512–520.
29. OttoSP, MarksJC (1996) Mating systems and the evolutionary transition between haploid and diploidy. Biol J Linnean Soc 57: 197–218.
30. HallDW (2000) The evolution of haploid, diploid and polymorphic haploid-diploid life cycles: the role of meiotic mutation. Genetics 156: 893–898.
31. OrrHA (1995) Somatic mutation favors the evolution of diploidy. Genetics 139: 1441–1447.
32. VicosoB, CharlesworthB (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7: 645–653.
33. WhitlockMC, AgrawalAF (2009) Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63: 569–582.
34. ConnallonT, CoxRM, CalsbeekR (2010) Fitness consequences of sex-specific selection. Evolution 64: 1671–1682.
35. MalletMA, BouchardJM, KimberCM, ChippindaleAK (2011) Experimental mutation-accumulation on the X chromosome of Drosophila melanogaster reveals stronger selection on males than females. BMC Evol Biol 11: 156.
36. SharpNP, AgrawalAF (2012) Male-biased fitness effects of spontaneous mutations in Drosophila melanogaster. Evolution DOI:10.1111/j.1558-5646.2012.01834.x.
37. BondurianskyR, ChenowethSF (2009) Intralocus sexual conflict. Trends Ecol Evol 24: 280–288.
38. van DoornGS (2009) Intralocus sexual conflict. Ann NY Acad Sci 1168: 52–71.
39. KidwellJF, CleggMT, StewartFM, ProutT (1977) Regions of stable equilibria for models of differential selection in the two sexes. Genetics 85: 171–183.
40. DayT, BondurianskyR (2004) Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167: 1537–1546.
41. IwasaY, PomiankowskiA (1999) Sex specific X chromosome expression caused by genomic imprinting. J Theor Biol 197: 487–495.
42. IwasaY, PomiankowskiA (2001) The evolution of X-linked genomic imprinting. Genetics 158: 1801–1809.
43. SeymourRM, PomiankowskiA (2006) ESS gene expression of X-linked imprinted genes subject to sexual selection. J Theor Biol 241: 81–93.
44. Van CleveJ, FeldmanMW (2007) Sex-specific viability, sex linkage and dominance in genomic imprinting. Genetics 176: 1101–1118.
45. MableBK, OttoSP (1998) The evolution of life cycles with haploid and diploid phases. Bio Essays 20: 453–462.
46. Otto SP, Day T (2007) A biologist's guide to mathematical modeling in ecology and evolution. Princeton University press, Princeton, NJ.
47. DobynsWB, FilauroA, TomsonBN, ChanAS, AllenWH, TingNT, OosterwijkJC, OberC (2004) Inheritance of most X-linked traits is not dominant or recessive, just X-linked. Am J Med Genet 129A: 136–143.
48. RavignéV, DieckmannU, OlivieriI (2009) Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat 174: E141–E169.
49. ConnallonT, ClarkAG (2011) The resolution of sexual antagonism by gene duplication. Genetics 187: 919–937.
50. GuillaumeF, OttoSP (2012) Gene functional trade-offs and the evolution of pleiotropy. Genetics 192: 1389–1409.
51. MankJE, VicosoB, BerlinS, CharlesworthB (2010) Effective population size and the faster-X effect: Empiricial results and their interpretation. Evolution 64: 663–674.
52. SantureAW, SpencerH (2012) Genomic imprinting leads to less selectively maintained polymorphism on X chromosomes. Genetics 192: 1455–1464.
53. CooperDW (1976) Studies on metatherian sex chromosomes II: the improbability of a stable balanced polymorphism at an X-linked locus with the paternal X inactivation system of kangaroos. Aust J Biol Sci 29: 245–250.
54. PattenMM, HaigD (2009) Maintenance or loss of genetic variation under sexual and parental antagonism at a sex-linked locus. Evolution 63: 2888–2895.
55. ConnallonT, ClarkAG (2012) A general population genetic framework for antagonistic selection that accounts for demography and recurrent mutation. Genetics 190: 1477–1489.
56. MullonC, PomiankowskiA, ReuterM (2012) The effects of selection and genetic drift on the genomic distribution of sexually antagonistic alleles. Evolution 66: 3743–3753.
57. MankJE, HoskenDJ, WedellN (2011) Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65: 2133–2144.
58. ChippindaleAK, GibsonJR, RiceWR (2001) Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci USA 98: 1671–1675.
59. FedorkaKM, MousseauTA (2004) Female mating bias results in conflicting sex-specific offspring fitness. Nature 429: 65–67.
60. FoersterK, CoulsonT, SheldonBC, PembertonJM, Clutton-BrockTH, KruukLEB (2007) Sexually antagonistic genetic variation for fitness in red deer. Nature 447: 1107–1110.
61. BrommerJE, KirkpatrickM, QvarnströmA, GustafssonL (2007) The intersexual genetic correlation for lifetime fitness in the wild and its implications for sexual selection. PLoS ONE 2: e744 doi:10.1371/journal.pone.0000744.
62. CoxRM, CalsbeekR (2010) Cryptic sex-ratio bias provides indirect genetic benefits despite sexual conflict. Science 328: 92–94.
63. InnocentiP, MorrowEH (2010) The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol 8: e1000335 doi:10.1371/journal.pbio.1000335.
64. MokkonenM, KokkoH, KoskelaE, LehtonenJ, MappesT, MartiskainenH, MillsSC (2011) Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus. Science 334: 972–974.
65. DelphLF, AndicoecheaJ, StevenJC, HerlihyCR, ScarpinoSV, BellDL (2011) Environment-dependent intralocus sexual conflict in a dioecious plant. New Phytologist 192: 542–552.
66. LewisZ, WedellN, HuntJ (2011) Evidence for strong intralocus sexual conflict in the Indian meal moth. Evolution 65: 2085–2097.
67. HaldaneJBS (1937) The effect of variation on fitness. Am Nat 71: 337–349.
68. SpencerHG, WilliamsMJM (1997) The evolution of genomic imprinting: two modifier-locus models. Theor Pop Biol 51: 23–35.
69. OttoSP, YongP (2002) The evolution of gene duplicates. Homol Eff 46: 451–483.
70. ConnallonT, ClarkAG (2010) Gene duplication, gene conversion and the evolution of the Y chromosome. Genetics 186: 277–286.
71. RiceWR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735–742.
72. BarlowDP (2011) Genomic imprinting: a mammalian epigenetic discovery model. Annu Rev Genet 45: 379–403.
73. SpencerHG, FeldmanMW, ClarkAG (1998) Genetic conflicts, multiple paternity and the evolution of genomic imprinting. Genetics 148: 893–904.
74. SpencerHG, ClarkAG, FeldmanMW (1999) Genetic conflicts and the evolutionary origin of genomic imprinting. Trends Ecol Evol 14: 197–201.
75. HaigD (2000) The kinship theory of genomic imprinting. Annu Rev Ecol Syst 31: 9–32.
76. WilkinsJF, HaigD (2003) What good is genomic imprinting: the function of parent specific gene expression. Nat Rev Genet 4: 359–368.
77. SpencerHG, FeldmanMW, ClarkAG, WeissteinAE (2004) The effect of genetic conflict on genomic imprinting and modification of expression at a sex-linked locus. Genetics 166: 565–579.
78. BrandvainY (2010) Matrisibs, patrisibs, and the evolution of imprinting on autosomes and sex chromosomes. Am Nat 176: 511–521.
79. BrandvainY, Van CleveJ, UbedaF, WilkinsJF (2011) Demography, kinship, and the evolving theory of genomic imprinting. Trends Genet 27: 251–257.
80. Maynard SmithM, PriceGR (1973) The logic of animal conflict. Nature 246: 15–18.
81. RozowskyJ, AbyzovA, WangJ, AlvesP, RahaD, HarmanciA, LengJ, BjornsonR, KongY, KitabayashiN, BhardwajN, RubinM, SnyderM, GersteinM (2011) AlleleSeq: analysis of allele-specific expression and binding in a network framework. Mol Syst Biol 7: 522.
82. ClercP, AvnerP (2006) Random X-chromosome inactivation: skewing lessons for mice and men. Curr Op Genet Dev 16: 246–253.
83. ThorvaldsenJL, KrappC, HuntingtonFW, BartolomeiMS (2012) Nonrandom X chromosome inactivation is influenced by multiple regions of the murine X chromosome. Genetics 192: 1095–1107.
84. OttoSP, BourguetD (1999) Balanced polymorphisms and the evolution of dominance. Am Nat 153: 561–574.
85. HoughJ, ImmlerS, BarrettSCH, OttoSP (2013) Evolutionary stable sex ratios and mutation load. Evolution in press.
86. AgrawalAF, WhitlockMC (2011) Inferences about the distribution of dominance drawn from yeast gene knockout data? Genetics 178: 553–566.
87. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York.
88. WeckerlyFW (1998) Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J Mammology 79: 33–52.
89. Lindenfors P, Gittleman JL, Jones KE (2007) Sexual size dimorphism in mammals. In Fairbairn DJ, Blanckenhorn WU, Székely T, eds. Sex, Size and Gender Roles, pp. 16–26. Oxford University Press, Oxford.
90. MukaiT (1969) The genetic structure of natural populations of Drosophila melanogaster. VIII. Natural selection on the degree of dominance of viability polygenes. Genetics 63: 467–478.
91. LandeR, SchemskeDW (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24–40.
92. CharlesworthB, CharlesworthD (1998) Some evolutionary consequences of deleterious mutations. Genetica 102/103: 3–19.
93. EllegrenH (2007) Characteristics, causes and evolutionary consequences of male-biased mutation. Proc Roy Soc B 274: 1–10.
94. SayresMA, MakovaKD (2011) Genome analyses substantiate male mutation bias in many species. Bioessays 33: 938–945.
95. HollisB, HouleD (2011) Populations with elevated mutation load do not benefit from the operation of sexual selection. J Evol Biol 24: 1918–1926.
96. ArbuthnottD, RundleHD (2012) Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster. Evolution 66: 2127–2137.
97. CoxRM, CalsbeekR (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173: 176–187.
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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