Homosexuality via canalized sexual development: A testing protocol for a new epigenetic model

BioEssays

Volumn 35, Issue 9, 2013, Pages 764-770

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

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Epigenetics; Gonad trait discordance; Homosexuality

Indexed keywords

ANDROGEN; TESTOSTERONE;

ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL LINEAGE; CELL TYPE; DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; FETAL STEM CELL; FETUS DEVELOPMENT; GENDER IDENTITY; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC MODEL; GENETIC POLYMORPHISM; GENETIC TRAIT; GLIA CELL; HETEROSEXUALITY; HOMOSEXUALITY; HOMOZYGOTE; HUMAN; HYPOTHESIS; KARYOTYPE 46,XX; KARYOTYPE 46,XY; MALE HOMOSEXUAL; MONOZYGOTIC TWINS; NEURAL STEM CELL; NULL ALLELE; PERINATAL PERIOD; PHENOTYPE; PREDICTION; PRENATAL PERIOD; SEX DIFFERENCE; SEXUAL DEVELOPMENT; SEXUAL ORIENTATION; SEXUALITY;

EPIGENETICS; GONAD-TRAIT DISCORDANCE; HOMOSEXUALITY;

EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOMOSEXUALITY; HUMANS; KARYOTYPE; MALE; MODELS, GENETIC; PHENOTYPE; POLYMORPHISM, GENETIC; TWINS;

EID: 84881610197     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300033     Document Type: Article

References (37)

1. Russell DGD, Sladen WJL, Ainley DG. 2012. Dr. George Murray Levick (1876-1956): unpublished notes on the sexual habits of the Adelie penguin. Polar Rec 48: 387-93.
2. Bagemihl B. 1999. Biological Exuberance: Animal Homosexuality and Natural Diversity. New York: St. Martin's Press.
3. Sommer V, Vasey PL. 2006. Homosexual Behaviour in Animals: An Evolutionary Perspective. New York: Cambridge University Press.
4. Poiani A. 2010. Animal Homosexuality: A Biosocial Perspective. New York: Cambridge University Press.
5. MacFarlane GR, Blomberg SP, Vasey PL. 2010. Homosexual behaviour in birds: frequency of expression is related to parental care disparity between the sexes. Anim Behav 80: 375-90.
6. Hunt GL Jr, Hunt MW. 1977. Female-female pairing in western gulls (Larus occidentalis) in southern California. Science 196: 1466-7.
7. Young LC, Zaun BJ, VanderWerf EA. 2008. Successful same-sex pairing in Laysan albatross. Biol Lett 4: 323-5.
8. Braithwaite LW. 1981. Ecological studies of the black swan. 3. Behavioral and social organization. Aust Wildlife Res 8: 135-46.
9. Kotrschal K, Hemetsberger J, Weiss B. 2006. Making the best of a bad situation: homosociality in male greylag geese. In Homosexual Behaviour in Animals. An Evolutionary Perspective. New York: Cambridge University Press, 45-76.
10. Ramagopalan SV, Dyment DA, Handunnetthi L, Rice GP, et al. 2010. A genome-wide scan of male sexual orientation. J Hum Genet 55: 131-2.
11. Bailey JM, Dunne MP, Martin NG. 2000. Genetic and environmental influences on sexual orientation and its correlates in an Australian twin sample. J Pers Soc Psychol 78: 524-36.
12. Savic I, Lindstrom P. 2008. PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects. Proc Natl Acad Sci USA 105: 9403-8.
13. Swaab DF. 2008. Sexual orientation and its basis in brain structure and function. Proc Natl Acad Sci USA 105: 10273-4.
14. Savic I, Berglund H, Lindstrom P. 2005. Brain response to putative pheromones in homosexual men. Proc Natl Acad Sci USA 102: 7356-61.
15. Berglund H, Lindstrom P, Savic I. 2006. Brain response to putative pheromones in lesbian women. Proc Natl Acad Sci USA 103: 8269-74.
16. Burke SM, Veltman DJ, Gerber J, Hummel T, et al. 2012. Heterosexual men and women both show a hypothalamic response to the chemo-signal androstadienone. PLoS ONE 7: e40993.
17. Roselli CE, Reddy RC, Kaufman KR. 2011. The development of male-oriented behavior in rams. Front Neuroendocrinol 32: 164-9.
18. Ngun TC, Ghahramani N, Sanchez FJ, Bocklandt S, et al. 2011. The genetics of sex differences in brain and behavior. Front Neuroendocrinol 32: 227-46.
19. Gavrilets S, Rice WR. 2006. Genetic models of homosexuality: generating testable predictions. Proc R Soc B-Biol Sci 273: 3031-8.
20. 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. Curr Pediatric Rev 4: 243-9.
21. Hines M. 2011. Prenatal endocrine influences on sexual orientation and on sexually differentiated childhood behavior. Front Neuroendocrinol 32: 170-82.
22. Franklin TB, Russig H, Weiss IC, Graff J, et al. 2010. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68: 408-15.
23. Morgan CP, Bale TL. 2011. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31: 11748-55.
24. Thornton J, Zehr JL, Loose MD. 2009. Effects of prenatal androgens on rhesus monkeys: a model system to explore the organizational hypothesis in primates. Horm Behav 55: 633-44.
25. Matsuda KI, Mori H, Kawata M. 2012. Epigenetic mechanisms are involved in sexual differentiation of the brain. Rev Endocr Metab Disord 13: 163-71.
26. Gardner DK, Larman MG, Thouas GA. 2010. Sex-related physiology of the preimplantation embryo. Mol Hum Reprod 16: 539-47.
27. 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: 563-70.
28. Dewing P, Shi T, Horvath S, Vilain E. 2003. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol Brain Res 118: 82-90.
29. Rice WR, Friberg U, Gavrilets S. 2012. Homosexuality as a consequence of epigenetically canalized sexual development. Q Rev Biol 87: 343-68.
30. Forest MG. 1985. Pitfalls in prenatal diagnosis of 21-hydroxylase deficiency by amniotic fluid steroid analysis? A six years experience in 102 pregnancies at risk. Ann NY Acad Sci 458: 130-47.
31. Heemers HV, Tindall DJ. 2007. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr Rev 28: 778-808.
32. Ollikainen M, Smith KR, Joo EJH, Ng HK, et al. 2010. DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet 19: 4176-88.
33. Arnold AP. 2012. The end of gonad-centric sex determination in mammals. Trends Genet 28: 55-61.
34. Ben-Yosef D, Amit A, Malcov M, Frumkin T, et al. 2011. Female sex bias in human embryonic stem cell lines. Hum Reprod 26: I348-I9.
35. Rosner M, Mikula M, Preitschopf A, Feichtinger M, et al. 2012. Neurogenic differentiation of amniotic fluid stem cells. Amino Acids 42: 1591-6.
36. Joo S, Ko IK, Atala A, Yoo JJ, et al. 2012. Amniotic fluid-derived stem cells in regenerative medicine research. Arch Pharm Res 35: 271-80.
37. Petit I, Kesner NS, Karry R, Robicsek O, et al. 2012. Induced pluripotent stem cells from hair follicles as a cellular model for neurodevelopmental disorders. Stem Cell Res 8: 134-40.