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Masculinization and Defeminization in Altricial and Precocial Mammals: Comparative Aspects of Steroid Hormone Action

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Masculinization and Defeminization in Altricial and Precocial Mammals: Comparative Aspects of Steroid Hormone Action 69 Masculinization and Defeminization in Altricial and Precocial Mammals: Comparative Aspects of Steroid Hormone Action Kim Wallen Michael J. Baum Department of Psychology and Yerkes Department of Biology Regional Primate Research Center Boston University Emory University Boston, Massachusetts Atlanta, Georgia Altricial and precocial species follow different devel- tween altricial and precocial species in the hormonal opmental trajectories possibly reflecting different re- actions producing masculinization and defeminization productive strategies. This chapter describes evidence might be an artifact of which species have become fa- that this distinction may have heuristic value in un- vored laboratory subjects. Alternatively, they may re- derstanding the nature of steroidal influences on mas- flect a deeper organizing principle resulting from the culinization and defeminization. Across both types of different life strategies of altricial and precocial species. mammals, defeminization was found to utilize estro- Resolving this issue awaits a broader comparative in- genic metabolites of androgens. However, the evidence vestigation of sexual differentiation than is currently of this requirement was stronger in altricial than preco- available today. cial species. Unambiguous evidence of defeminization Phoenix et al. (1959) closed their landmark paper by nonaromatizable androgens was found only in the proposing that steroid hormones organized the sex- precocial rhesus monkey. The role of aromatization in ual characteristics of the developing nervous system masculinization was less clear, with little evidence in with the following: “We are assuming that testosterone any species that mounting potential differentiated un- or some metabolite acts on these central nervous tis- der either androgenic or estrogenic influence. When all sues in which patterns of sexual behavior are orga- aspects of male sexual and social behavior were con- nized.” This caution concerning whether testosterone sidered, altricial species relied more on aromatization (T) or its metabolites were the active agents in orga- for masculinization than did precocial species. No ev- nizing the nervous system has assumed a central po- idence was found in human males that the actions of sition in the 40 years of research following the paper’s estrogenic compounds were necessary for normal male publication. While the Kansas group might have been sexual differentiation. These apparent differences be- cautious about which steroid was responsible for CNS Hormones, Brain and Behavior Copyright C 2002, Elsevier Science (USA). VOLUME FOUR 385 All rights reserved. 386 IV. Development of Hormone-Dependent Neuronal Systems organization, they certainly did not foresee an era when culine and suppress feminine characteristics. Although the dominant view would be that estrogenic metabolites this developmental cascade from gene expression to go- of androgens are the primary steroids organizing behav- nadal differentiation, leading to hormone production, ioral sexual differentiation in mammals. The discovery and finally to morphological and behavioral differentia- that neural tissues, particularly the hypothalamus, in tion encompasses the principle pathway by which sex- some mammals contained the enzymes necessary to ual differentiation occurs, evidence suggests that there aromatize androgens to estrogen raised the possibil- may be nonhormonal ways in which the sex determin- ity that high circulating levels of androgens might be ing genes affect sexual differentiation (Arnold, 1996). regionally converted to estrogens, altering neural de- For example, evidence from mice suggests that the Sry velopment. This notion, which came to be called the gene is transcribed in the developing male, but not fe- aromatization hypothesis, went from being counter- male, brain raising the possibility of a direct effect of intuitive to becoming a central tenet of sexual differ- Sry transcripts on neural organization (Lahr et al., 1995; entiation. However, its centrality may reflect an acci- Mayer et al., 2000). While these findings are intriguing dent of the species that dominate laboratory studies and demonstrate that a full description of the sexual of sexual differentiation. When sexual differentiation is differentiation process is likely to contain surprises, it explored from a comparative perspective, it is unclear is apparent that the actions of testicular hormones play that aromatization is involved in the sexual differentia- a large and critical role in sexual differentiation. This tion of all species. Furthermore, even for those species role, specifically of steroid hormones, is the focus of where aromatization has been demonstrated to be im- this chapter. We first briefly describe the cascade of dif- portant it is not clear that it is required for all aspects ferentiating events that testicular hormones influence. of behavioral sexual differentiation. Mammalian sexual differentiation is biased in a fe- This chapter describes evidence from a broad range of male direction ( Jost, 1970). By this we mean that mor- mammalian species of the involvement, or lack thereof, phogenic processes are geared to producing female end- of estrogenic metabolites in behavioral sexual differenti- points in sexual differentiation more easily than they ation. In particular, we investigate the role of aromatized produce male endpoints. Some have thus referred to metabolites of androgens in the processes of masculin- the female path of differentiation as the default path, ization and defeminization of behavior and explore the meaning it is the pattern that most easily occurs. Un- possibility that species differences in the role of estro- fortunately, others have equated default with passive or genic metabolites may reflect the relative completeness inactive and the term has become politicized and lost of sexual differentiation at birth. its original sense that masculine characteristics are im- posed on an essentially female life-plan ( Jost, 1970). This concept is valuable as it implies that the failure of I. BASIC PROCESSES OF BEHAVIORAL a process necessary to produce a male trait leads to the SEXUAL DIFFERENTIATION creation of a female phenotypic trait instead. The con- verse is not true; that when a female process is blocked, Mammalian males and females have different sex a male characteristic arises. Thus, while there can be no chromosomes, and sexual differentiation results from doubt that female differentiation requires a suite of ac- a cascade of events that result from the expression tive morphogenic processes, it is also the case that male of genes on these chromosomes, as well as autoso- differentiation requires two specific processes that allow mal genes (Swain and Lovell-Badge, 1999). Current the male phenotype to alter what is essentially female- evidence supports the view that products of the Sry biased differentiation. gene on the Y chromosome interact with the X chro- The nomenclature used to describe sexual differenti- mosome genes, Sox9, and autosomal genes to cause ation has been historically quite confusing, using, often the undifferentiated fetal gonad to become a testicle with little precision, terms such as feminization and instead of an ovary (Koopman, 1999). Gonadal differ- demasculinization. It is now apparent that two pro- entiation then sets in motion a series of events in which cesses are necessary to create a male; masculinization testicular hormones direct the differentiation of mas- and defeminization. Masculinization imposes malelike 69. Masculinization and Defeminization in Altricial and Precocial Mammals 387 characters on the developing organism, whereas de- ence of penis, scrotum, testes, and internal Wolffian feminization suppresses femalelike characteristics that duct derivatives. Behaviorally, we limit our discus- would otherwise arise. These processes are involved sion to male-typical copulatory behavior and partner- whether the endpoints are anatomical or behavioral and preference, except in monkeys, where masculine pat- can operate in concert or independently. The original terns of juvenile behavior are described. notion for these processes came from anatomical in- vestigations of sexual differentiation and is modeled af- B. Defeminization ter anatomical processes differentiating the primordial duct systems into male or female internal reproductive This term refers to the suppression of female-typical organs. characteristics. Anatomically this results in the suppres- Prior to gonadal differentiation, males and females sion of the development of uterus, fallopian tubes, por- possess both Mullerian¨ and Wolffian duct systems, tions of the vagina, and vaginal opening. Behaviorally, which give rise, respectively, to the internal female and defeminization suppresses sexual receptivity, termed male nongonadal reproductive structures. These inter- receptive defeminization. In monkeys, defeminization nal nongonadal reproductive structures arise from sep- appears to suppress interest in sexual initiation, termed arate primordial structures, and thus errors in sexual proceptive defeminization. differentiation allow either or both duct derivatives to exist concurrently, or derivatives from neither duct structure. This is in contrast to other reproductive II. DEVELOPMENTAL STAGE AT BIRTH structures, such as the gonad or the external genitalia, AND SEXUAL DIFFERENTIATION in which a single bipotential primordium differentiates into either a male or a female endpoint, and a failure of Species vary widely
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