Sexually antagonistic epigenetic marks that canalize sexually dimorphic development

Molecular Ecology

Volumn 25, Issue 8, 2016, Pages 1812-1822

  Rice, William R ^a   Friberg, Urban ^b   Gavrilets, Sergey ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LINKÖPING UNIVERSITY   (Sweden)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

canalization; epigenetics; gonad trait discordance; sex specific epimarks; sexual conflict; sexual dimorphism; transgenerational epigenetics

Indexed keywords

ANIMAL; FEMALE; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MAMMAL; MUTATION; SEXUAL DEVELOPMENT;

ANIMALS; EPIGENESIS, GENETIC; FEMALE; MALE; MAMMALS; MUTATION; SEX CHARACTERISTICS;

EID: 84955161763     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13490     Document Type: Article

References (76)

1. Arnqvist G, Rowe L, (1995) Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proceedings of the Royal Society of London B: Biological Sciences, 261, 123-127.
2. Arnqvist G, Rowe L, (2005) Sexual Conflict. Princeton University Press, Princeton, New Jersey, USA.
3. Arnqvist G, Vellnow N, Rowe L, (2014) The effect of epistasis on sexually antagonistic genetic variation. Proceedings of the Royal Society of London B: Biological Sciences, 281, 20140489.
4. Bailey JM, Dunne MP, Martin NG, (2000) Genetic and environmental influences on sexual orientation and its correlates in an Australian twin sample. Journal of Personality and Social Psychology, 78, 524-536.
5. Banovich NE, Lan X, McVicker G, et al,. (2014) Methylation QTLs are associated with coordinated changes in transcription factor binding, histone modifications, and gene expression levels.
6. Bay K, Main KM, Toppari J, Skakkebæk NE, (2011) Testicular descent: INSL3, testosterone, genes and the intrauterine milieu. Nature Reviews Urology, 8, 187-196.
7. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A, (2008) Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiological Genomics, 32, 264-272.
8. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A, (2010) Sex determines the expression level of one-third of the actively expressed genes in bovine blastocysts. Proceedings of the National Academy of Sciences, 107, 3394-3399.
9. Bermejo-Alvarez P, Rizos D, Lonergan P, Gutierrez-Adan A, (2011) Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction, 141, 563-570.
10. Bogaert AF, Skorska M, (2011) Sexual orientation, fraternal birth order, and the maternal immune hypothesis: a review. Frontiers in Neuroendocrinology, 32, 247-254.
11. Boisen K, Chellakooty M, Schmidt I, et al,. (2005) Hypospadias in a cohort of 1072 Danish newborn boys: prevalence and relationship to placental weight, anthropometrical measurements at birth, and reproductive hormone levels at three months of age. The Journal of Clinical Endocrinology & Metabolism, 90, 4041-4046.
12. Cantor JM, Blanchard R, Paterson AD, Bogaert AF, (2002) How many gay men owe their sexual orientation to fraternal birth order? Archives of Sexual Behavior, 31, 63-71.
13. Carmina E, (1998) Prevalence of idiopathic hirsutism. European Journal of Endocrinology, 139, 421-423.
14. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L, (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature, 373, 241-244.
15. Choudhry S, Deshpande A, Qiao L, et al,. (2012) Genome-wide DNA methylation profiling of CpG islands in hypospadias. The Journal of Urology, 188, 1450-1456.
16. Dewing P, Shi T, Horvath S, Vilain E, (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Molecular Brain Research, 118, 82-90.
17. Fang H, Tong W, Branham WS, et al,. (2003) Study of 202 natural, synthetic, and environmental chemicals for binding to the androgen receptor. Chemical Research in Toxicology, 16, 1338-1358.
18. Fiddler M, Abdel-Rahman B, Rappolee DA, Pergament E, (1995) Expression of SRY transcripts in preimplantation human embryos. American Journal of Medical Genetics, 55, 80-84.
19. Fouse SD, Shen Y, Pellegrini M, et al,. (2008) Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell, 2, 160-169.
20. Franklin TB, Russig H, Weiss IC, et al,. (2010) Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408-415.
21. Fry JD, (2010) The genomic location of sexually antagonistic variation: some cautionary comments. Evolution, 64, 1510-1516.
22. Gardner DK, Larman MG, Thouas GA, (2010) Sex-related physiology of the preimplantation embryo. Molecular Human Reproduction, 16, 539-547.
23. Gavrilets S, Arnqvist G, Friberg U, (2001) The evolution of female mate choice by sexual conflict. Proceedings of the Royal Society of London B: Biological Sciences, 268, 531-539.
24. Gebert C, Wrenzycki C, Herrmann D, et al,. (2009) DNA methylation in the IGF2 intragenic DMR is re-established in a sex-specific manner in bovine blastocysts after somatic cloning. Genomics, 94, 63-69.
25. Haldane JBS, (1926) A mathematical theory of natural and artificial selection. Part III. Proceedings of the Cambridge Philosophical Society, 23, 363-372.
26. Hall CM, Jones JA, Meyer-Bahlburg HF, et al,. (2004) Behavioral and physical masculinization are related to genotype in girls with congenital adrenal hyperplasia. The Journal of Clinical Endocrinology & Metabolism, 89, 419-424.
27. Hemberger M, Dean W, Reik W, (2009) Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nature Reviews Molecular Cell Biology, 10, 526-537.
28. Hines M, (2011) Prenatal endocrine influences on sexual orientation and on sexually differentiated childhood behavior. Frontiers in Neuroendocrinology, 32, 170-182.
29. Ho DH, Burggren WW, (2010) Epigenetics and transgenerational transfer: a physiological perspective. The Journal of Experimental Biology, 213, 3-16.
30. Hotchkiss AK, Lambright CS, Ostby JS, et al,. (2007) Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague-Dawley rats. Toxicological Sciences, 96, 335-345.
31. Imperato-Mcginley J, Peterson RE, Gautier T, Sturla E, (1979) Male pseudohermaphroditism secondary to 5α-reductase deficiency-a model for the role of androgens in both the development of the male phenotype and the evolution of a male gender identity. Journal of Steroid Biochemistry, 11, 637-645.
32. Karabulut R, Turkyilmaz Z, Sonmez K, et al,. (2013) Twenty-four genes are upregulated in patients with hypospadias. Balkan Journal of Medical Genetics, 16, 39-43.
33. Kidwell J, Clegg M, Stewart F, Prout T, (1977) Regions of stable equilibria for models of differential selection in the two sexes under random mating. Genetics, 85, 171-183.
34. Łebkowska M, Załȩska-Radziwiłł M, (2007) Endocrine disruptors-ecotoxicological assays. Archiwum Ochrony Środowiska, 33, 81-88.
35. Lee AJ, Mitchem DG, Wright MJ, et al,. (2014) Genetic factors that increase male facial masculinity decrease facial attractiveness of female relatives. Psychological Science, 25, 476-484.
36. Lees-Murdock DJ, Walsh CP, (2008) DNA methylation reprogramming in the germ line. In: Genomic Imprinting (ed., Wilkins JF,), pp. 1-15. Springer, New York.
37. Li Y, Zheng M, Lau Y-FC, (2014) The sex-determining factors SRY and SOX9 regulate similar target genes and promote testis cord formation during testicular differentiation. Cell Reports, 8, 723-733.
38. Lowe R, Gemma C, Rakyan VK, Holland ML, (2015) Sexually dimorphic gene expression emerges with embryonic genome activation and is dynamic throughout development. BMC Genomics, 16, 295.
39. Mandel SPH, (1971) Owens model of a genetical system with differential viability between sexes. Heredity, 26, 49-63.
40. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK, (2012) Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS ONE, 7, e31901.
41. Meselson M, Stahl FW, (1958) The replication of DNA in Escherichia coli. Proceedings of the National Academy of Sciences, 44, 671-682.
42. Meyer-Bahlburg HF, (2005) Gender identity outcome in female-raised 46, XY persons with penile agenesis, cloacal exstrophy of the bladder, or penile ablation. Archives of Sexual Behavior, 34, 423-438.
43. Mikkelsen TS, Ku M, Jaffe DB, et al,. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 448, 553-560.
44. Mitchem DG, Purkey AM, Grebe NM, et al,. (2014) Estimating the sex-specific effects of genes on facial attractiveness and sexual dimorphism. Behavior Genetics, 44, 270-281.
45. Morgan CP, Bale TL, (2011) Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. Journal of Neuroscience, 31, 11748-11755.
46. New MI, (2004) An update of congenital adrenal hyperplasia. Annals of the New York Academy of Sciences, 1038, 14-43.
47. Ngun TC, Ghahramani N, Sanchez FJ, Bocklandt S, Vilain E, (2011) The genetics of sex differences in brain and behavior. Frontiers in Neuroendocrinology, 32, 227-246.
48. Nugent BM, Wright CL, Shetty AC, et al,. (2015) Brain feminization requires active repression of masculinization via DNA methylation. Nature Neuroscience, 18, 690-697.
49. Ostby J, Monosson E, Kelce WR, Gray LE, (1999) Environmental antiandrogens: low doses of the fungicide vinclozolin alter sexual differentiation of the male rat. Toxicology and Industrial Health, 15, 48-64.
50. Parker G, (1979) Sexual selection and sexual conflict. In: Sexual Selection and Reproductive Competition in Insects (eds, Blum MS, Blum NA,), pp. 123-166. Academic Press, New York.
51. Penaloza CG, Estevez B, Han DM, et al,. (2014) Sex-dependent regulation of cytochrome P450 family members Cyp1a1, Cyp2e1, and Cyp7b1 by methylation of DNA. The FASEB Journal, 28, 966-977.
52. Perera DMD, McGarrigle HHG, Lawrence DM, Lucas M, (1987) Amniotic-fluid testosterone and testosterone glucuronide levels in the determination of fetal sex. Journal of Steroid Biochemistry and Molecular Biology, 26, 273-277.
53. Reik W, Dean W, Walter J, (2001) Epigenetic reprogramming in mammalian development. Science, 293, 1089-1093.
54. Reiner WG, Gearhart JP, (2004) Discordant sexual identity in some genetic males with cloacal exstrophy assigned to female sex at birth. New England Journal of Medicine, 350, 333-341.
55. Rey RA, Grinspon RP, (2011) Normal male sexual differentiation and aetiology of disorders of sex development. Best Practice & Research Clinical Endocrinology & Metabolism, 25, 221-238.
56. Reyes FI, Borodits RS, Winter JSD, Faiman C, (1974) Studies on human sexual development. 2. Fetal and maternal serum gonadotropin and sex steroid concentrations. Journal of Clinical Endocrinology & Metabolism, 38, 612-617.
57. Rice WR, (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution, 38, 735-742.
58. Rice WR, (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature, 381, 232-234.
59. Rice WR, Gavrilets S, (2014) The Genetics and Biology of Sexual Conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
60. Rice WR, Holland B, (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behavioral Ecology and Sociobiology, 41, 1-10.
61. Rice WR, Friberg U, Gavrilets S, (2012) Homosexuality as a consequence of epigenetically canalized sexual development. Quarterly Review of Biology, 87, 343-368.
62. Rice WR, Friberg U, Gavrilets S, (2013) Homosexuality via canalized sexual development: a testing protocol for a new epigenetic model. BioEssays, 35, 764-770.
63. Rice WR, Gavrilets S, (2014) The Genetics and Biology of Sexual Conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
64. Sanders A, Martin E, Beecham G, et al,. (2015) Genome-wide scan demonstrates significant linkage for male sexual orientation. Psychological Medicine, 45, 1379-1388.
65. Sax L, (2002) How common is intersex? A response to Anne Fausto-Sterling. Journal of Sex Research, 39, 174-178.
66. Sekido R, (2014) The potential role of SRY in epigenetic gene regulation during brain sexual differentiation in mammals. Advances in Genetics, 86, 135-165.
67. Silversides DW, Raiwet DL, Souchkova O, Viger RS, Pilon N, (2012) Transgenic mouse analysis of Sry expression during the pre-and peri-implantation stage. Developmental Dynamics, 241, 1192-1204.
68. Skinner MK, Guerrero-Bosagna C, (2014) Role of CpG deserts in the epigenetic transgenerational inheritance of differential DNA methylation regions. BMC Genomics, 15, 692.
69. Speiser PW, White PC, (2003) Congenital adrenal hyperplasia. New England Journal of Medicine, 349, 776-788.
70. Thornton J, Zehr JL, Loose MD, (2009) Effects of prenatal androgens on rhesus monkeys: a model system to explore the organizational hypothesis in primates. Hormones and Behavior, 55, 633-644.
71. Trakakis E, Loghis C, Kassanos D, (2009) Congenital adrenal hyperplasia because of 21-hydroxylase deficiency: a genetic disorder of interest to obstetricians and gynecologists. Obstetrical & Gynecological Survey, 64, 177-189.
72. Tsankov AM, Gu H, Akopian V, et al,. (2015) Transcription factor binding dynamics during human ES cell differentiation. Nature, 518, 344-349.
73. Watson JD, Crick FHC, (1953a) Molecular structure of nucleic acids. Nature, 171, 737-738.
74. Watson JD, Crick FHC, (1953b) Genetic implications of the structure of deoxyribonucleic acid. Nature, 171, 964-967.
75. Weisz J, Ward IL, (1980) Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology, 106, 306-316.
76. Wisniewski AB, Kirk KD, Copeland KC, (2008) Long-term psychosexual development in genetic males affected by disorders of sex development (46, XY DSD) reared male or female. Current Pediatric Reviews, 4, 243-249.