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Is it useful to view the brain as a secondary sexual characteristic?

Ball, Gregory F.; Balthazart, Jacques; McCarthy, Margaret M.

2014 • In Neuroscience and Biobehavioral Reviews, 46 Pt 4, p. 628-38

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https://hdl.handle.net/2268/181820

DOI
10.1016/j.neubiorev.2014.08.009

PubMed
25195165

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Keywords :

Female competition; Organizing effects of steroids; Sex differences; Sexual differentiation; Sexual selection; Sexually differentiated gene expression

Abstract :

[en] Many sex differences in brain and behavior related to reproduction are thought to have evolved based on sexual selection involving direct competition for mates during male-male competition and female choice. Therefore, certain aspects of brain circuitry can be viewed as secondary sexual characteristics. The study of proximate causes reveals that sex differences in the brain of mammals and birds reflect organizational and activational effects of sex steroids as articulated by Young and collaborators. However, sex differences in brain and behavior have been identified in the cognitive domain with no obvious link to reproduction. Recent views of sexual selection advocate for a broader view of how intra-sexual selection might occur including such examples as competition within female populations for resources that facilitate access to mates rather than mating competition per se. Sex differences can also come about for other reasons than sexual selection and recent work on neuroendocrine mechanisms has identified a plethora of ways that the brain can develop in a sex specific manner. Identifying the brain as sexually selected requires careful hypothesis testing so that one can link a sex-biased aspect of a neural trait to a behavior that provides an advantage in a competitive mating situation.

Disciplines :

Animal psychology, ethology & psychobiology
Neurosciences & behavior

Author, co-author :

Ball, Gregory F.

Balthazart, Jacques ; Université de Liège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

McCarthy, Margaret M.

Language :

English

Title :

Is it useful to view the brain as a secondary sexual characteristic?

Publication date :

2014

Journal title :

Neuroscience and Biobehavioral Reviews

ISSN :

0149-7634

eISSN :

1873-7528

Publisher :

Elsevier, United Kingdom

Volume :

46 Pt 4

Pages :

628-38

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Copyright (c) 2014 Elsevier Ltd. All rights reserved.

Available on ORBi :

since 22 May 2015

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134

Bibliography

Adkins E.K. Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol. 1975, 89:61-71.
Adkins E.K. Embryonic exposure to an antiestrogen masculinizes behavior of female quail. Physiol. Behav. 1976, 17:357-359.
Adkins E.K. Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. Neuroendocrinology 1979, 29:178-185.
Adkins E.K., Adler N.T. Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol. 1972, 81:27-36.
Agate R.J., Grisham W., Wade J., Mann S., Wingfield J., Schanen C., Palotie A., Arnold A.P. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc. Natl. Acad. Sci. USA 2003, 100:4873-4878.
Amateau S.K., McCarthy M.M. A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J. Neurosci. 2002, 22:8586-8596.
Amateau S.K., McCarthy M.M. Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat. Neurosci. 2004, 7:643-650.
Andersson M. Sexual Selection 1994, Princeton University Press, Princeton, NJ.
Arnold A.P., Chen X. What does the four core genotypes mouse model tell us about sex differences in the brain and other tissues?. Front. Neuroendocrinol. 2009, 30:1-9.
Arnold A.P., Gorski R.A. Gonadal steroid induction of structural sex differences in the central nervous system. Ann. Rev. Neurosci. 1984, 7:413-442.
Auger A.P., Olesen K.M. Brain sex differences and the organisation of juvenile social play behaviour. J. Neuroendocrinol. 2009, 21:519-525.
Bachtrog D., Mank J.E., Peichel C.L., Kirkpatrick M., Otto S.P., Ashman T.L., Hahn M.W., Kitano J., Mayrose I., Ming R., Perrin N., Ross L., Valenzuela N., Vamosi J.C., Tree of Sex Consortium Sex determination: why so many ways of doing it?. PLoS Biol. 2014, 12:e1001899.
Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat. Neurosci. 2006, 9:220-226.
Bakker J., Honda S., Harada N., Balthazart J. The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J. Neurosci. 2002, 22:9104-9112.
Ball G.F., Balthazart J. Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 2008, 363:1699-1710.
Ball G.F., Sockman K.W., Duffy D.L., Gentner T.Q. A neuroethological approach to song behavior and perception in European starlings: interrelationships among testosterone, neuroanatomy, immediate early gene expression, and immune function. Adv. Study Anim. Behav. 2006, 36:59-63.
Balthazart J. Hormonal correlates of behavior. Avian Biology 1983, vol. VII:221-365. Academic Press, New York.
Balthazart J. Minireview: hormones and human sexual orientation. Endocrinology 2011, 152:2937-2947.
Balthazart J. The Biology of Homosexuality 2012, Oxford University Press, New York.
Balthazart J., Arnold A.P., Adkins-Regan E. Sexual differentiation of brain and behavior in birds. Hormones, Brain and Behavior 2009, 1745-1787. Academic Press, San Diego, CA. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
Balthazart J., Ball G.F. Sexual differentiation of brain and behavior in birds. Trends Endocrinol. Metab. 1995, 6:21-29.
Balthazart J., De Clerck A., Foidart A. Behavioral demasculinization of female quail is induced by estrogens: studies with the new aromatase inhibitor, R76713. Horm. Behav. 1992, 26:179-203.
Balthazart J., Schumacher M., Ottinger M.A. Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen. Comp. Endocrinol. 1983, 51:191-207.
Balthazart J., Young L.M. Mate selection, sexual orientation and pair bonding. Knobil and Neill's Physiology of Reproduction 2014, Elsevier, Taramani, India. fourth ed. T. Plant, T. Zelenik (Eds.).
Becker J.B., Berkley K.J., Geary N., Hampson E., Herman J.P., Young E.A. Sex Differences in the Brain. From Genes to Behavior 2008, Oxford, Oxford University Press.
Benbow C.P. Sex differences in mathematical reasoning ability in intellectually talented preadolescents: their nature, effects and possible causes. Behav. Brain Sci. 1988, 11:169-183.
Benbow C.P., Lubinski D. Consequences of gender differences in mathematical reasoning ability and some biological linkages. The Development of Sex Differences and Similariies in Behavior 1993, 87-109. NATO ASI Series, Dordrecht. M. Haug, R.E. Whalen, C. Aron, K.L. Olsen (Eds.).
Berta P., Hawkins J.R., Sinclair A.H., Taylor A., Griffiths B.L., Goodfellow P.N., Fellous M. Genetic evidence equating SRY and the testis-determining factor. Nature 1990, 348:448-450.
Biswal B.B., Mennes M., Zuo X.N., Gohel S., Kelly C., Smith S.M., Beckmann C.F., Adelstein J.S., Buckner R.L., Colcombe S., Dogonowski A.M., Ernst M., Fair D., Hampson M., Hoptman M.J., Hyde J.S., Kiviniemi V.J., Kotter R., Li S.J., Lin C.P., Lowe M.J., Mackay C., Madden D.J., Madsen K.H., Margulies D.S., Mayberg H.S., McMahon K., Monk C.S., Mostofsky S.H., Nagel B.J., Pekar J.J., Peltier S.J., Petersen S.E., Riedl V., Rombouts S.A., Rypma B., Schlaggar B.L., Schmidt S., Seidler R.D., Siegle G.J., Sorg C., Teng G.J., Veijola J., Villringer A., Walter M., Wang L., Weng X.C., Whitfield-Gabrieli S., Williamson P., Windischberger C., Zang Y.F., Zhang H.Y., Castellanos F.X., Milham M.P. Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4734-4739.
Breedlove S.M., Arnold A.P. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 1980, 210:564-566.
Brock O., Baum M.J., Bakker J. The development of female sexual behavior requires prepubertal estradiol. J. Neurosci. 2011, 31:5574-5578.
Butler J. Gender Trouble: Feminism and the Subversion of Identity 1990, Routledge, New York.
Cahill L. Why sex matters for neuroscience. Nat. Rev.: Neurosci. 2006, 7:477-484.
Cahill L. Sex influences on brain and emotional memory: the burden of proof has shifted. Prog. Brain Res. 2010, 186:29-40.
Cahill L. Fundamental sex difference in human brain architecture. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:577-578.
Cameron N.M., Fish E.W., Meaney M.J. Maternal influences on the sexual behavior and reproductive success of the female rat. Horm. Behav. 2008, 54:178-184.
Carranza J. Defining sexual selection as sex-dependent selection. Anim. Behav. 2009, 77:749-751.
Catchpole C.K., Slater P.J.B. Bird Song. Biological Themes and Variations 2008, Cambridge, UK, Cambridge University Press.
Champagne F.A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 2008, 29:386-397.
Chung W.C., De Vries G.J., Swaab D.F. Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood. J. Neurosci. 2002, 22:1027-1033.
Clutton-Brock T. What is sexual selection?. Sexual Selection in Primates: New and Comparative Perspectives 2004, 24-36. Cambridge University Press, Cambridge. P. Kappeler, C. Van Schaik (Eds.).
Clutton-Brock T. Sexual selection in males and females. Science 2007, 318:1882-1885.
Clutton-Brock T., Huchard E. Social competition and its consequences in female mammals. J. Zool. 2013, 289:151-171.
Clutton-Brock T.H., Huchard E. Social competition and selection in males and females. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2013, 368. 20130074.
Darwin C. The Descent of Man and Selection in Relation to Sex 1871, John Murray, London.
De Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 2002, 22:9005-9014.
Deisseroth K., Feng G., Majewska A.K., Miesenbock G., Ting A., Schnitzer M.J. Next-generation optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 2006, 26:10380-10386.
Dewing P., Shi T., Horvath S., Vilain E. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res. Mol. Brain Res. 2003, 118:82-90.
Döhler K.D. More evidence for the role of estrogens in female differentiation of the brain. Behav. Brain Sci. 1998, 21:329-330.
Döhler K.D., Hancke J.L., Srivastava S.S., Hofman C., Shryne J.E., Gorski R.A. Participation of estrogens in female sexual differentiation of the brain; neuroanatomical, neuroendocrine and behavioral evidence. Prog. Brain Res. 1984, 61:99-117.
Drury J.P., Gowaty P.A. Social selection, sexual selection, and sexual conflict. Encyclopedia of Animal Behavior 2010, 273-280. Academic Press, Oxford. M.D. Breed, J. Moore (Eds.).
Du S., Itoh N., Askarinam S., Hill H., Arnold A.P., Voskuhl R.R. XY sex chromosome complement, compared with XX, in the CNS confers greater neurodegeneration during experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:2806-2811.
Duffy D.L., Bentley G.E., Ball G.F. Does sex or photoperiodic condition influence ZENK induction in response to song in European starlings?. Brain Res. 1999, 844:78-82.
Eens M., Pinxten R., Verheyen R.F. Male song as a cue for mate choice in the European startling. Behaviour 1991, 116:210-238.
Ellis L., Hershberger S., Field E., Wersinger S., Pelis S., Geary D., Palmer C., Hoyenga K., Hetsroni A., Karadi K. Sex Differences: Summarizing more than a Century of Scientific Research 2008, Psychology Press, New York.
Erskine M.S., Lehmann M.L., Cameron N.M., Polston E.K. Co-regulation of female sexual behavior and pregnancy induction: an exploratory synthesis. Behav. Brain Res. 2004, 153:295-315.
Fisher R.A. The Genetical theory of Natural Selection 1930, Clarendon, Oxford, UK.
Fortune E.S., Rodriguez C., Li D., Ball G.F., Coleman M.J. Neural mechanisms for the coordination of duet singing in wrens. Science 2011, 334:666-670.
Gentner T.Q., Hulse S.H., Duffy D., Ball G.F. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J. Neurobiol. 2001, 46:48-58.
Gioiosa L., Chen X., Watkins R., Umeda E.A., Arnold A.P. Sex chromosome complement affects nociception and analgesia in newborn mice. J. Pain 2008, 9:962-969.
Gorski R.A. Gonadal hormones and the perinatal development of neuroendocrine function. Frontiers in Neuroendocrinology 1971, 237-290. Oxford University Press, New York. L. Martini, W.F. Ganong (Eds.).
Gorski R.A., Gordon J.H., Shryne J.E., Southam A.M. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 1978, 148:333-346.
Guiso L., Monte F., Sapienza P., Zingales L. Diversity. Culture, gender, and math. Science 2008, 320:1164-1165.
Hall Z.J., MacDougall-Shackleton S.A., Osorio-Beristain M., Murphy T.G. Male bias in the song control system despite female bias in song rate in streak-backed orioles (Icterus pustulatus). Brain, Behav. Evol. 2010, 76:168-175.
Hines M. Sex Steroids and Human Behavior: Prenatal Androgen Exposure and Sex-Typical Play Behavior in Children. Ann. N. Y. Acad. Sci. 2003, 1007:272-282.
Hines M. Brain Gender 2004, Oxford University Press, Oxford.
Hyde J.S., Lindberg S.M., Linn M.C., Ellis A.B., Williams C.C. Diversity. Gender similarities characterize math performance. Science 2008, 321:494-495.
Imwalle D.B., Bateman H.L., Wills A., Honda S., Harada N., Rissman E.F. Impairment of spatial learning by estradiol treatment in female mice is attenuated by estradiol exposure during development. Horm. Behav. 2006, 50:693-698.
Ingalhalikar M., Smith A., Parker D., Satterthwaite T.D., Elliott M.A., Ruparel K., Hakonarson H., Gur R.E., Gur R.C., Verma R. Sex differences in the structural connectome of the human brain. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:823-828.
Jacobs L.F. Sexual selection and the brain. Trends Ecol. Evol. 1996, 11:82-86.
Jordan-Young R.M. Brain Storm. The Flaws in the Science of Sex Differences 2010, Harvard University Press, Cambridge, MA.
Jost A. A new look at the mechanisms controlling sex differentiation in mammals. Johns Hopkins Med. J. 1972, 130:38-53.
Kelley D. Sexually dimorphic behaviors. Ann. Rev. Neurosci. 1988, 11:225-251.
Kimura D. Sex, sexual orientation and sex hormones influence human cognitive function. Curr. Opin. Neurobiol. 1996, 6:259-263.
Kimura D. Human sex differences in cognition, fact, not predicament. Sex. Evol. Gender 2004, 6:45-53.
Krebs-Kraft D.L., Hill M.N., Hillard C.J., McCarthy M.M. Sex difference in cell proliferation in developing rat amygdala mediated by endocannabinoids has implications for social behavior. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20535-20540.
Leitner S., Voigt C., Metzdorf R., Catchpole C.K. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 2005, 64:275-284.
Lenz K.M., Nugent B.M., McCarthy M.M. Sexual differentiation of the rodent brain: dogma and beyond. Front. Neurosci. 2012, 6:26.
Lenz K.M., Sengelaub D.R. Maternal licking influences dendritic development of motoneurons in a sexually dimorphic neuromuscular system. Brain Res. 2006, 1092:87-99.
LeVay S., Valente S.M. Human sexuallity 2006, Sinauer Associates Inc., Sunderland, MA.
MacDougall-Shackleton S.A., Ball G.F. Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci. 1999, 22:432-436.
MacDougall-Shackleton S.A., MacDougall-Shackleton E.A., Hahn T.P. Physiological and behavioural responses of female mountain white-crowned sparrows to natal- and foreign-dialect songs. Can. J. Zool. 2001, 79:325-333.
Maney D.L., MacDougall-Shackleton E.A., MacDougall-Shackleton S.A., Ball G.F., Hahn T.P. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J. Comp. Physiol. A 2003, 189:667-674.
McCarthy M.M., De Vries G.J., Forger N.G. Sexual differentiation of the brain: mode, mechanisms, and meaning. Hormones, Brain and Behavior 2009, 1707-1746. Academic Press, San Diego, CA. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
McCarthy M.M. A lumpers versus splitters approach to sexual differentiation of the brain. Front. Neuroendocrinol. 2011, 32:114-123.
McCarthy M.M., Arnold A.P., Ball G.F., Blaustein J.D., De Vries G.J. Sex differences in the brain: the not so inconvenient truth. J. Neurosci. 2012, 32:2241-2247.
McCarthy M.M., Besmer H.R., Jacobs S.C., Keidan G.M., Gibbs R.B. Influence of maternal grooming, sex and age on Fos immunoreactivity in the preoptic area of neonatal rats: implications for sexual differentiation. Dev. Neurosci. 1997, 19:488-496.
McCarthy M.M., Schwarz J.M., Wright C.L., Dean S.L. Mechanisms mediating oestradiol modulation of the developing brain. J. Neuroendocrinol. 2008, 20:777-783.
McCarthy M.M., Wright C.L., Schwarz J.M. New tricks by an old dogma: mechanisms of the organizational/activational hypothesis of steroid-mediated sexual differentiation of brain and behavior. Horm. Behav. 2009, 55:655-665.
Meaney M.J. The sexual differentiation of social play. Trends Neurosci. 1988, 11:54-58.
Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann. Rev. Neurosci. 2001, 24:1161-1192.
Meaney M.J., Szyf M. Maternal care as a model for experience-dependent chromatin plasticity?. Trends Neurosci. 2005, 28:456-463.
Moore C.L. The Role of Maternal Stimulation in the Development of Sexual Behavior and its Neural Basis. Ann. N. Y. Acad. Sci. 1992, 662:160-177.
Moore C.L., Chadwick-Dias A.M. Behavioral responses of infant rats to maternal licking: variations with age and sex. Dev. Psychobiol. 1986, 19:427-438.
Moore C.L., Dou H., Juraska J.M. Maternal stimulation affects the number of motor neurons in a sexually dimorphic nucleus of the lumbar spinal cord. Brain Res. 1992, 572:52-56.
Moore C.L., Power K.L. Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring. Dev. Psychobiol. 1992, 25:165-182.
Noble R.G., Attas A., Adler N.T. The control of sexual behavior in the female hamster. Hormones and Behaviour in Higher Vertebrates 1983, 325-341. Springer Verlag, Berlin. J. Balthazart, E. Pröve, R. Gilles (Eds.).
Nottebohm F., Arnold A.P. Sexual dimorphism in vocal control areas of the songbird brain. Science 1976, 194:211-213.
Panzica G.C., Viglietti-Panzica C., Balthazart J. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 1996, 17:51-125.
Pasterski V.L., Geffner M.E., Brain C., Hindmarsh P., Brook C., Hines M. Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev. 2005, 76:264-278.
Peterson M.P., Rosvall K.A., Taylor C.A., Lopez J.A., Choi J.H., Ziegenfus C., Tang H., Colbourne J.K., Ketterson E.D. Potential for sexual conflict assessed via testosterone-mediated transcriptional changes in liver and muscle of a songbird. J. Exp. Biol. 2014, 217:507-517.
Phoenix C.H., Goy R.W., Gerall A.A., Young W.C. Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
Reisert I., Pilgrim C. Sexual differentiation of monoaminergic neurons - genetic or epigenetic?. Trends Neurosci. 1991, 14:468-473.
Renfree M.B., Harry J.L., Shaw G. The marsupial male: a role model for sexual development. Philos. Trans. R. Soc. Lond. [Biol.] 1995, 350:243-251.
Renfree M.B., Pask A.J., Shaw G. Sex down under: the differentiation of sexual dimorphisms during marsupial development. Reprod. Fertil. Dev. 2001, 13:679-690.
Roselli C.E., Larkin K., Resko J.A., Stellflug J.N., Stormshak F. The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology 2004, 145:478-483.
Rosvall K.A. Intrasexual competition in females: evidence for sexual selection. Behav. Ecol. 2011, 22:1131-1140.
Ruigrok A.N., Salimi-Khorshidi G., Lai M.C., Baron-Cohen S., Lombardo M.V., Tait R.J., Suckling J. A meta-analysis of sex differences in human brain structure. Neurosci. Biobehav. Rev. 2014, 39:34-50.
Schwarz J.M., Liang S.L., Thompson S.M., McCarthy M.M. Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences. Neuron 2008, 58:584-598.
Schwarz J.M., McCarthy M.M. The role of neonatal NMDA receptor activation in defeminization and masculinization of sex behavior in the rat. Horm. Behav. 2008, 54:662-668.
Schwarz J.M., McCarthy M.M. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J. Neurochem. 2008, 105:1561-1572.
Sherry D.F., Forbes M.R., Khurgel M., Ivy G.O. Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:7839-7843.
Sherry D.F., Hampson E. Evolution and the hormonal control of sexually dimorphic spatial abilities in humans. Trends Cogn. Sci. 1997, 1:50-56.
Short R.V. Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes. Adv. Study Behav. 1979, 9:131-158.
Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., Foster J.W., Frischauf A.M., Lovell-Badge R., Goodfellow P.N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990, 346:240-244.
Smith C.A., Roeszler K.N., Ohnesorg T., Cummins D.M., Farlie P.G., Doran T.J., Sinclair A.H. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
Spelke E.S. Sex differences in intrinsic aptitude for mathematics and science? A critical review. Am. Psychol. 2005, 60:950-958.
Stockley P., Bro-Jorgensen J. Female competition and its evolutionary consequences in mammals. Biol. Rev. 2011, 86:341-366.
Thor D.H., Holloway W.R. Social play soliciting by male and female juvenile rats: effects of neonatal androgenization and sex of cagemates. Behav. Neurosci. 1986, 100:275-279.
Vallet E., Kreutzer M. Female canaries are sexually responsive to special song phrases. Anim. Behav. 1995, 49:1603-1610.
Wade J., Arnold A.P. Sexual Differentiation of the Zebra Finch Song System. Ann. N. Y. Acad. Sci. 2004, 1016:540-559.
Wallen K., Hassett J.M. Sexual differentiation of behaviour in monkeys: role of prenatal hormones. J. Neuroendocrinol. 2009, 21:421-426.
Weber D., Skirbekk V., Freund I., Herlitz A. The changing face of cognitive gender differences in Europe. Proc. Natl. Acad. Sci. U. S. A. 2014, 10.1073/pnas.1319538111.
Wiedenheft B., Sternberg S.H., Doudna J.A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 2012, 482:331-338.
Wright C.L., McCarthy M.M. Prostaglandin E2-induced masculinization of brain and behavior requires protein kinase A, AMPA/kainate, and metabotropic glutamate receptor signaling. J. Neurosci. 2009, 29:13274-13282.
Wright C.L., Schwarz J.S., Dean S.L., McCarthy M.M. Cellular mechanisms of estradiol-mediated sexual differentiation of the brain. Trends Endocrinol. Metab. 2010, 21:553-561.

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