Sexual Orientation: Toward Biological Understanding.

Sexual Orientation: Toward Biological Understanding. Edited by Lee Ellis and Linda Ebertz. Westport, CT: Praeger, 1997, 276 pages. Cloth, $65.00.

Books such as Sexual Orientation: Toward Biological Understanding have an important role in influencing both the scientific and general public's perception of just how important biology is in sexual behavior. Masterfully edited by Ellis and Ebertz, this volume brings together 11 of the 60 presentations made at the "First International Behavioral Development Symposium: Biological Basis of Sexual Orientation and Sex-Typical Behavior" held at Minor State University in 1995. The Minor conference was decidedly impressive, bringing together the world's leading sex researchers to reaffirm the pre-eminence of biology to sexual behavior. As stated by the editors, "A fundamental premise upon which the conference was organized is that sexual orientation and sex-typical behavior patterns can be fully understood only within a biological context" (p. ix). This volume is the first of two based on the conference. The central theme of this volume is the biological basis of sexual orientation. The second volume will center on sex-typical behavior. Other presentations from the conference were published in a special issue of the The Journal of Sex Research.

Beginning with a foreword by Brian Gladue establishing the steady rise in research and publication activity concerned with biological aspects of sexual orientation over the last few decades, the book is divided into two parts: (a) genetic and perinatal influences on sexual orientation, and (b) neurological and physiological aspects of sexual orientation.

Genetic and perinatal influences on sexual orientation. The first chapter in this section, by Matthew Grober, describes sexual differentiation in fish, a vertebrate species much underused for providing insights into mammalian sexual biology. Fish are notable for their sexual plasticity, or the ability to change sexual phenotype. The species of fish discussed in this chapter, the bluehead wrasse, exhibits both unidirectional sex change and multiple male phenotypes. Depending on surrounding social conditions, hormonal reactions are stimulated which can cause an initial phase male fish to change either to a female phenotype or a terminal phase male phenotype. Terminal males are the dominant and largest males in the social group, and are the males responsible for breeding. Much of the chapter is devoted to describing the social conditions and hormonal conditions that lead to sexual phenotype changes. The benefit of using fish as a model tot mammalian sexual physiology rests in the similarity of their brain areas and neuroendocrine functions that control the development and maintenance of sexual behavior. Grober makes a compelling case for the usefulness of fish in understanding mammalian sexuality, noting that in both wrasses and primates individuals are sensitive to social status, social status and increased population density affects reproduction through stress, multiple phenotypes are present within a sex, environmental variation generates variation in the social system, brain structures are correlated with variation in sexual phenotype, and complete behavioral sex reversal takes place. Wrasses are unique in the sense that complete gonadal sex reversal can take place. Grober's work is fascinating, and I predict that much useful knowledge concerning human sexuality will result from it.

The chapter by Kinsely, Lambert, and Jones approaches a topic that is noncontroversial in nonhuman animals but is highly controversial in humans: Prenatal exposure to stress affects the sexual differentiation of the male fetus. This chapter basically reviews the work of the authors and others demonstrating that in species of male mice, maternal prenatal stress affects the fetuses' exposure to levels of sex hormones, and consequentially, the development of the nervous system. More dramatically, stress also leads to both demasculinization and feminization in adulthood. Demasculinization is characterized by difficulty in ejaculation; feminization by a lordotic response. The evidence for the affects of prenatal stress on female fetuses is scantier, although a masculinizing affect has been shown. Issues similar to those for using fish as a model for human sexuality arise with using mice as a model of human sexuality. Because extensive literature exists on this topic, I will not even attempt a review of the arguments used both for and against the validity of the mouse model. Unlike fish, mice are not virgin territory. Suffice it to say that questioning the validity of the mouse model is a favorite strategy of researchers hostile to biological models of human sexual behavior. This criticism is as alive today as it was two decades ago, despite the many known parallels between the sexual neuroanatomy of the mouse and human brains. Nonetheless, it is incumbent on the authors to generally discuss these criticisms, and more specifically, to discuss how applicable the stress hypothesis is to human sexual orientation. Unfortunately, the authors do not do a good job in this respect: Less than two pages are devoted to discussing the hypothesis' generalizability to other species and strains (pp. 28-29). In this space, Kinsley et al. briefly mention human studies of prenatal stress. This does not do justice to a highly complex area of research, a complete recitation of which would lead one to see that prenatal stress does affect male sexual orientation in humans. The reason for the omission may be due to Ellis' chapter, which discusses at length the effects of prenatal and perinatal factors on sex-typical development.

Humans are the experimental organisms in Meyer-Bahlburg's chapter on the effects of prenatal estrogen on sexual orientation. The primary reason why findings from nonhuman animals are often of ambiguous applicability to humans is that the same experimental manipulations studied in animals cannot be done in humans. Thus, researchers utilize experiments of nature in which, in utero, the individual is exposed to unusual hormonal patterns. Although the evidence is clear in mice that estrogens are important for the defeminization of the brain, it is less clear in humans. The purpose of Bahlburg's chapter is to review the evidence both for and against the role of estrogens in the sexual differentiation of the human brain. Bahlburg concludes that the evidence is highly contradictory. On the one hand, elevated rates of bisexuality and homosexuality in women exposed prenatally to the estrogen diethylstilbestrol (DES) confirm the role of estrogen. On the other hand, 46 XY individuals with complete androgen insensitivity syndrome (cAIS) who still respond to estrogens are identified as women and speak against the defeminizing role of estrogens. This chapter is made particularly interesting by introducing two newly-discovered hormonal conditions that have some pertinence to the estrogen issue: an estrogen receptor deficiency syndrome and an aromatase deficiency syndrome that results in estrogen deprivation, both in males. Both of these conditions would lead to the prediction that a lack of masculinization would occur. However, two case studies reported no support for this conclusion. Although Bahlburg concludes that the support for estrogen in influencing human sexual orientation is unclear, knowledge of the history in this area suggests that as sample sizes and the number of studies increase, so will the clarity. This clarity is exemplified by the case of congenital adrenal hyperplasia.

Building on Bahlburg's chapter is Dittmann's chapter on one specific hormonal disorder, congenital adrenal hyperplasia (CAH), in which the fetus is exposed to an excess of androgens. Most CAH patients are of two types: simple virilizers (SV) or salt-wasters (SW) who, in addition to excessive androgen exposure, have difficulty in metabolizing sodium chloride, leading to dangerous levels of dehydration. The expectation is that CAH patients will exhibit more masculine characteristics. Dittmann's chapter focuses on females: CAH in males does not lead to any apparent effects. The author's review of his own research and the research of others indisputably shows that CAH is associated with the masculinization of many characteristics in females: Elevated rates of "tomboyism," aggression, typical masculine preferences, and female homosexuality are usually found. In addition, as the severity of the condition rises (SW as opposed to SV), so does the masculinization. One might even dare to say that the relation between CAH and masculinization is causal, because carefully conducted studies have shown that the association is there even without overt physical masculinization and without the patient's knowledge of the condition. CAH is one of the true research success stories in the biology of human sexuality. This success only came about through the commitment of many researchers to replicate and expand on the work of others. This commitment will ultimately result in the same success in the area of estrogen and human sexuality.

Ellis' chapter is a review of prenatal and perinatal influences on sex-typical development in nonhuman animals, and to a lesser extent, humans. Ellis does an impressive job of summarizing the vast amount of evidence within the confines of a short chapter. There is no doubt that prenatally certain drugs, diseases, alcohol, tobacco, and maternal stress affect the behavior of both humans and nonhumans. In humans, the evidence that prenatal mishaps, such as maternal exposure to heavy metals, affect behaviors that are sex-linked (an elevated rate of aggression) is indirect. In nonhumans, the link is direct, as in the association between maternal alcohol exposure and adult sexual behavior in rats. As noted by Ellis, this research suggests a number of intriguing hypotheses that have yet to be tested; for instance, that the sex-typical behavior of children exposed prenatally to alcohol will differ from others.

Neurological and physiological aspects of sexual orientation. Bakker and Slob's chapter complements Bahlburg's by reviewing the important role estrogen plays in adult male rat sexual partner preference (or motivational aspects of sexual behavior). This is a somewhat different approach than that taken by other authors, who focus on actual coital performance. Perhaps it is also a more pertinent approach with respect to generalizing to humans. Most of the results reported in this chapter were obtained from studies that prenatally or neonatally administered aromatase inhibitor (ATD). In summary, neonatally-treated ATD male rats show a mixture of homosexual and heterosexual partner preferences. The inclusion of this chapter in the neurological and physiological aspects part of the book comes from the profound affects of ATD on several neural structures: the vasopressin content of the suprachiasmatic nucleus (SCN) and the volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA). More vasopression is found in ATD-treated rats, resulting in more nocturnal fluctuations in partner preference, and the volume of the SDN-POA is smaller in ATD-treated rats, associated with, paradoxically it seems, more responsiveness to heterosexual partner preferences (although still retaining some homosexual preferences not present in non-ATD-treated male rats). Could this phenomenon (e.g., a bisexual partner preference in male rats) serve as a model for the same phenomenon in humans? The authors do not explore this possibility, but it would have been interesting to have a formal discussion of this issue, given the almost complete absence of any biological theorizing in support of bisexuality.

Where the Bakker and Slob chapter leaves off, the chapter by Swaab, Zhou, Fodor, and Hofman picks up. Bakker and Slob are concerned with the association between neural structures and sexual partner preference in rats; Swaab et al. are concerned with the same association in humans. These researchers document differences in hypothalmic and other limbic structures associated with sex and sexual orientation. Differences found related to sex include the SDN-POA, the interstitial nucleus of the anterior hypothalamus (INAH-2 and INAH-3), the bed nucleus of the stria terminalis (BST), the SCN, the anterior commissure, and the interthalamic adhesion. Differences found related to sexual orientation also include the SCN, INAH-3, anterior commissure, and, in addition, the isthmus of the corpus callosum. The brain structures of homosexual men tend to lie in size and volume between (heterosexual) male and female brain structures. Some of the human anatomical differences are homologous to differences in rats (SDN-POA), although others are not (INAH-2 and INAH3). There are at least two major contributions made by this exceptionally clearly written chapter. The first is to add some semantic clarity to an area that often lacks it; for example, the authors point out that four different names are used in the literature for what is called the "SDN-POA." The second is to suggest reasons why results sometimes do not replicate across the few studies which have been done. Undoubtedly, studies concerned with neuroanatomical comparisons between heterosexuals and homosexuals will continue to increase in number. The hope is that there will be greater attempts to include females, and that experimental and histological procedures across studies will be standardized.

Perking and Fitzgerald's chapter disproves the false but prevalent notion that homosexuality does not exist naturally among nonhuman species: that when homosexuality is exhibited, it is a result of captivity. The authors demonstrate, within the wild and outside of it, that some domestic adult male rams are exclusively homosexual in orientation. In some senses, both the Grober chapter and this one are revolutionary: Both justify the use of their respective (and unusual) animal models by establishing the many parallels between fish and ram neurological and neuroendocrinological functioning on the one hand, and human neurological and neuroendocrinological functioning on the other. This conservation of biological function and structure is truly remarkable.

If a list was created of the most reliable differences found between homosexuals and heterosexuals, handedness would probably be fourth in replicability after gender conformity (both male and female homosexuals less), birth order (male homosexuals but not female homosexuals later born), and weight differences (male homosexuals lighter, female homosexuals heavier). In terms of handedness differences, both male and female homosexuals are presumed to have higher rates of left-handedness. This replicability, however, is not usually apparent. Holtzen's chapter on sexual orientation and handedness attempts to remedy this by pointing out the many flaws that are common to most studies, and by presenting the results of his own study. As with many research areas in sexual orientation, consistent results are much stronger for males than females. Sexual orientation-handedness association may be seen as an interesting, albeit a rather trivial, research endeavor. This thinking is incorrect, for handedness is probably one of the best clues to cerebral (hence cognitive) organization. Handedness is also associated with a host of other individual difference characteristics, including learning, autoimmunological functioning, and cognitive abilities.

The chapter by Herman-Jelinska, Dulko, and Grabowska extends the sexual orientation-handedness association to transsexuals where, in both male-to-female and female-to-male transsexuals, elevated rates of left-handedness are expected. Note that finding a transsexuality-handedness association transcends the sexual orientation-handedness association because many transsexuals are heterosexual. This implies that the brain areas responsible for sexual behavior are different from the areas responsible for sexual identity.

One of the most fascinating areas currently in vogue in sexual orientation research is the examination of sexual orientation differences in cognitive abilities. That is, do homosexuals and heterosexuals differ on various cognitive abilities? Halpern and Crothers tackle this issue by writing a chapter which locates several measures which typically show sex differences (i.e., verbal analogies, mental rotation, arithmetic, verbal fluency tasks). Finding that homosexual and heterosexual men and women differ on a number of cognitive abilities that also show differences between men and women supports a hormonal theory of sexual orientation. A hormonal theory predicts that homosexual men show a pattern of performance closer to that of heterosexual women, and that homosexual women show a pattern of performance closer to that of heterosexual men. The authors compare three groups: heterosexual men, homosexual men, and heterosexual women; thus, their findings are only pertinent to a male sexual orientation comparison. Their results are in conflict with prior prediction: Homosexuals do not perform poorer on tests which typically show male superiority. Rather, homosexuals respond in the typical male direction but are more extreme. As admitted by Halpern and Crothers, it is difficult to interpret why their results contradict the results of other studies. Although results can be highly contradictory in this area, heterosexual male superiority on mental rotation tasks has been well-replicated. An obvious difference between this study and others is a failure to use the same measures. Researchers in this area would be well served to begin doing so. Also, as with many areas of research in sexual orientation, lesbians are underrepresented. Difficulties in recruiting lesbians is not a good enough reason not to include them. There are other places in this book where not including lesbians restricts the biological conclusions to only males.

An objective reading of Sexual Orientation: Toward Biological Understanding suggests even to the most skeptical reader the power of biology in influencing sexual orientation. I do not mean to imply that contradictory, ambiguous, or disconfirmatory results do not exist among the biological findings. But the general message of the power of biology is so strong it transcends these obfuscating details. This in large measure is due to Ellis and Ebertz, who are to be congratulated for keeping true to their promise, given in the preface, of making the book readable to nonspecialists. Anyone interested in the current state of research into the biological origins of sexual orientation can do no better than to read this book.

Scott L. Hershberger, Ph.D., California State University, Department of Psychology, 250 Bellflower Blvd., Long Beach, CA 90840; e-mail: [e-mail]