Reframing sexual differentiation of the brain by Margaret M McCarthy & Arthur P Arnold in Nature Neuroscience 14, 677–683 (2011)
In the twentieth century, the dominant model of sexual differentiation stated that genetic sex (XX versus XY) causes differentiation of the gonads, which then secrete gonadal hormones that act directly on tissues to induce sex differences in function. This serial model of sexual differentiation was simple, unifying and seductive. Recent evidence, however, indicates that the linear model is incorrect and that sex differences arise in response to diverse sex-specific signals originating from inherent differences in the genome and involve cellular mechanisms that are specific to individual tissues or brain regions. Moreover, sex-specific effects of the environment reciprocally affect biology, sometimes profoundly, and must therefore be integrated into a realistic model of sexual differentiation. A more appropriate model is a parallel-interactive model that encompasses the roles of multiple molecular signals and pathways that differentiate males and females, including synergistic and compensatory interactions among pathways and an important role for the environment.
See also: From Fertilization to Adult Sexual Behavior by Milton Diamond, Teresa Binstock, & James V Kohl in Hormones and Behaviour, 30, 333-353 (1996)
Research has established the broad mammalian developmental plan that genes on the sex chromosomes influence gonad development which determines gonadal hormone production (or its absence) leading to modification of the genitalia and simultaneously biasing the nervous system to organize adult sexual behavior. This might be considered the “gonad to hormones to behavior” model. It is clear, however, that although this model generally works well it is incomplete. The model does not account for behavioral influences attributed to the environment or to genetic but nongonadal or hormonal factors. In this essay we probe those areas of sexual development that are neither differentiated by hormones nor activated by them. The concept of the environment used for our discussion is very broad; it incorporates considerations of both the molar and the molecular levels. The general sense of the word “environment” as something exterior to the person is retained, even if that something influences intraperson processes. In addition, we focus directly on molecular events themselves. Here the “environment” involved can be that within a DNA segment. We also expand the notion of “biologically based sex differences.” Although many, and perhaps most, important sex differences arise from gonadal and hormonal development, also important are sex differences which are neither gonadal nor hormonal. All these factors affect the internal workings of the individual and intervene in structuring how the social environment might or might not modify sexual behavior. This discourse calls attention to features that are central to the so-called nature-nurture discussion.
I have written or co-authored two other articles that detail how the social environment influences sexual behavior, and how it influences sexual orientation. However, not everyone recognizes that mammalian pheromones are social odors, which makes them social influences. For example: Simon LeVay wrote “The book on social influences is not closed so much as it is blank.” From mice to men: Biological factors in the development of sexuality. Levay S. Front Neuroendocrinol. 2011 Apr;32(2):110-3.
Given current opinions about what pheromones are and what they do, I suspect that the problem is my inability to convey the message that pheromones are social odors/social influences. (see: Human pheromones: integrating neuroendocrinology and ethology. Kohl JV, Atzmueller M, Fink B, Grammer K. Neuro Endocrinol Lett. (2001). Oct;22(5):309-21. Review and The Mind’s Eyes: Human pheromones, neuroscience, and male sexual preferences. Journal of Psychology & Human Sexuality. (2007)18 (4) 313-369.
I hope to better convey the message that food odors and social odors influence the same basic neurophysiological mechanism (i.e., the GnRH pulse), which allows them to alter the gene-cell-tissue-organ-organ system pathway which links them to hormones and behavior. Clearly, to me, the sex differences in social odors is the driving biological force behind postnatal sexual differentiation and the development of sexual orientation. It should become just as clear that we are not likely to see dramatic stereotypical effects from exposure either to food odors or to social odors. Associated behaviors develop; they are not innate, and genetically predisposed responses require stimulus presentation (e.g., from the environment).