Sex and seasonal differences in aggression and steroid secretion in Lemur catta: Are socially dominant females hormonally ‘masculinized’?
Introduction
Unlike most mammals (Ralls, 1976), many strepsirrhine primates display a social organization that is characterized by female dominance over males (Jolly, 1966, Richard, 1987). This unusual trait has received considerable attention and its behavioral regulation has engendered significant debate: Some researchers suggest that males defer to females only in feeding contexts, via ‘male deference’ (Hrdy, 1981) or ‘female feeding priority’ (Jolly, 1984), whereas others suggest that females maintain elevated status through overt aggression against males, via ‘female dominance’ (Kappeler, 1990a, Pereira et al., 1990). Regardless of the gradations in intersexual social relationships, functional explanations for the evolution of this trait, that invoke benefits to the female, are often linked to reproductive energetics, maternal investment, or nutritional intake (Jolly, 1984, Richard and Nicoll, 1987, Tilden and Oftedal, 1995, Young et al., 1990); nevertheless, the proximate mechanism remains a mystery.
Insight into a potential mechanism of female social dominance may derive from other unusual features of strepsirrhines, including sexual size monomorphism (Kappeler, 1990b), absence of bimaturation (Leigh and Terranova, 1998), and ambiguous (Hill, 1953, Ioannou, 1971, Petter-Rousseaux, 1964) or moderately ‘masculinized’ (Drea and Weil, submitted for publication) external genitalia. This array of male-like behavioral, physiological, and morphological traits calls attention to the possible role of androgens in female lemur development. Although female animals display aggression in a variety of social contexts, the neuroendocrine mechanisms that govern female competitive behavior remain poorly understood. Consequently, using the ringtailed lemur (Lemur catta) as a model – one with evolutionary ties to humans – I examine a potential route of hormonal mediation in female aggression and explore the hypothesis that female strepsirrhines may be masculinized by endogenous androgens.
An hormonal mechanism of social dominance ideally could explain an entire suite of male-like characteristics in the female, as well as patterns of individual or species variation. For instance, contemporary understanding of sexual differentiation requires that androgens circulate in the female fetus to produce male-like genitalia (Jost, 1953). Female exposure to prenatal androgens also delays puberty in the masculine direction (Goy and Robinson, 1982). Finally, androgens might enhance female aggressiveness, and hence dominance, by functioning as organizing hormones during fetal life or activating hormones in adulthood (Beatty, 1979, Goy and McEwen, 1980, MacLusky and Naftolin, 1981). Here, I explore the potential activating role of steroids in female aggression, recognizing that a contemporaneous hormone–behavior relationship is also affected by earlier organizational influences.
The suite of masculine traits in female lemurs recalls another exceptional mammal—the female spotted hyena (Crocuta crocuta). For instance, the external genitalia of female L. catta vaguely resemble those of the male, i.e. in terms of enlargement and elongation of the clitoris, as well as clitoral placement of the urinary meatus (Drea and Weil, submitted for publication). Likewise, but more strikingly, the external genitalia of female Crocuta closely mimic those of the male: The clitoris is elongated to form a fully erectile pseudopenis and the labia are permanently fused to form a pseudoscrotum (Frank et al., 1990, Matthews, 1939, Neaves et al., 1980). Thus, female Crocuta are unique among mammals in that they lack an external vagina and require mating and parturition to occur through a urogenital canal that traverses the hypertrophied clitoris. Importantly, the present discussion addresses only the shared morphological characteristics between the external genitalia of female lemurs and hyenas.
In addition, male and female L. catta mature at similar ages (Sussman, 1991) and achieve similar adult sizes (Drea and Weil, in preparation, Kappeler, 1990b). Somewhat more unusually, female Crocuta mature later than do males and achieve greater mass (Glickman et al., 1992, Kruuk, 1972, Matthews, 1939). In both species, which live in ‘multimale–multifemale’ societies (L. catta: Jolly, 1966, Sussman, 1991; Crocuta: Frank, 1986, Kruuk, 1972), females unconditionally dominate their male companions (L. catta: Jolly, 1966, Kappeler, 1990a, Pereira et al., 1990, Sauther, 1993; Crocuta: Drea and Frank, 2003, Frank, 1986, Kruuk, 1972, Smale et al., 1993). Thus, both species have promiscuous mating systems in which females exercise significant reproductive control (Drea and Wallen, 2003, Drea et al., 1999, East et al., 1993, Sauther, 1991) and gain other advantages, such as priority of access to resources.
Unlike in strepsirrhines, for which there is a dearth of hormonal data, the reproductive endocrinology of the spotted hyena has received considerable attention. Beyond the contribution of androgen-independent mechanisms to genital development (Drea et al., 1998, Glickman et al., 1998, Glickman et al., 2006), sexual differentiation in the female spotted hyena has both a prenatal and a postnatal hormone component, reflected by elevated androgen concentrations during the fetal period and throughout life (Dloniak et al., 2004, Drea et al., 1998, Glickman et al., 1987, Glickman et al., 1992, Licht et al., 1992, Licht et al., 1998, Lindeque et al., 1986, Racey and Skinner, 1979). Prior investigators identified the prohormone Δ4 androstenedione (Androst-4-ene-3,17,dione; A4) as the primary circulating androgen in the female spotted hyena and established that females have higher circulating concentrations of A4 than do males, more than 90% of which has an ovarian source (Glickman et al., 1987, Glickman et al., 1992, Licht et al., 1992, Racey and Skinner, 1979). Although typically dismissed as a weak or inactive androgen because it fails to bind to androgen receptors, A4 is readily converted to either testosterone (T) or estrone in the presence of appropriate enzymes. Free A4 is therefore an ideal substrate for local conversion to active androgens and estrogens, either of which could produce powerful effects on behavior and morphology.
Several lines of evidence link A4 to female dominance in spotted hyenas. For instance, the hyena placenta is characterized by high 17β-hydroxy-dehydrogenase activity, which converts A4 to T. Increasing plasma T levels in pregnant females are transferred to developing fetuses of both sexes, providing a mechanism for female expression of male-typical traits (Licht et al., 1992, Licht et al., 1998, Yalcinkaya et al., 1993). Mothers with the highest androgen concentrations during pregnancy produce the most aggressive offspring (Dloniak et al., 2006), whereas anti-androgen treated mothers (Drea et al., 1998) produce infants that show both reduced A4 concentrations and less severe sibling aggression during the early postnatal period (Drea et al., unpublished data). Lastly, ovariectomy during the juvenile period significantly reduces female aggression towards males in adult life, implicating an activational role of ovarian hormones, including either androgens and/or estrogens, in female dominance (Baker, 1990).
The behavioral and morphological similarities between female Crocuta and L. catta support a comparative endocrine approach to define factors relevant to feminine development, independent of phylogenetic constraints. In early studies of lemur reproductive endocrinology, researchers assessed hormone concentrations from serum or plasma samples (Bogart et al., 1977, Evans and Goy, 1968, Van Horn and Resko, 1977, Van Horn et al., 1976), whereas current investigators typically rely on hormone assays derived from fecal preparations (Cavigelli and Pereira, 2000, Von Engelhardt et al., 2000). In both cases, the investigators report on steroid production either in only one sex or for only a portion of the year, such that comparative data on the full reproductive cycle are unavailable. With one exception (Von Engelhardt et al., 2000), investigators also follow traditional paradigms, focused on assessing the role either of estrogens and progestogens in regulating female reproductive cycles (Bogart et al., 1977, Van Horn and Resko, 1977) or of T in regulating male reproductive cycles and aggression (Bogart et al., 1977, Cavigelli and Pereira, 2000, Evans and Goy, 1968, Van Horn et al., 1976). There are no reports on measurement of A4 in either sex. In the present study, I obtained serum samples from adult lemurs of both sexes throughout the entire annual cycle, repeated for four breeding seasons. During the last two years, I also obtained data on social behavior, focusing on aggressive interactions. I report on both sex-typical (e.g. 17β-estradiol, E2, in females) and sex-atypical or ‘heterologous’ (e.g. A4 and T in females) hormones.
In the present study, I examine on the bioavailability of A4 to female lemurs. In spotted hyenas, adult, nonpregnant females have circulating A4 concentrations that are elevated by comparison to (1) their own T concentrations, (2) A4 concentrations of male conspecifics, and (3) A4 concentrations of many other female mammals (Glickman et al., 1992). According to the present hypothesis, if A4 is implicated in female dominance, the same general patterns should be evident in adult, nonpregnant female lemurs. Because ‘masculinization’ is less extreme in lemurs than in spotted hyenas, however, an important caveat is that these patterns may be less pronounced in lemurs. Moreover, if seasonal A4 elevations occur in lemurs, they should be most apparent during periods characterized by heightened aggression. An additional goal of this study is to track correlated seasonal changes in steroid concentrations as a possible indicator of the major metabolic pathway involved in T production. If A4 provides the main source of T via the progesterone or Δ4-pathway, as opposed to the dehydroepiandrosterone or Δ5-pathway, then animals should show a positive correlation in the production of these two androgens (Wichmann et al., 1984).
Section snippets
Animals
The subjects of the endocrine study were 22 captive-born, gonadally intact ringtailed lemurs, including 10 females (age range: 2–20 years) and 12 males (age range: 2.5–20 years; Table 1). These animals were the adult members of three semi-free ranging social groups housed at the Duke Lemur Center (DLC), in Durham, NC (see housing details below). I studied the animals during four periods: an 8-month period from Dec 1999 to Jul 2000, a 6-month period from Oct 2001 to Mar 2002, and two contiguous
Sex differences in steroid production
Ringtailed lemurs showed clear sex differences in androgen production (Fig. 1). On average, serum concentrations of both A4 and T were significantly elevated in males by comparison to females (A4: t20 = 3.370, P < 0.005; T: t20 = 7.297, P < 0.001). Male A4 and T concentrations also appeared to be elevated by comparison to other non-lemurid species (Table 2). Whereas T concentrations were far (26x) greater in males than in females, A4 concentrations in males were less than double (1.7×) those of females
Discussion
To enhance our understanding of the processes regulating feminine development and to gain insight into the evolution of female social dominance in Malagasy lemurs, I explored the possibility that both natural sex–role reversal (i.e. female display of masculine behavioral traits) and genital mimicry (i.e. female display of masculine morphological traits) characteristic of this lineage might be associated with ‘heterologous’ hormones (i.e. female production of androgens) in adult animals. More
Acknowledgments
S. Cork, C. Fitzpatrick, K.R. Grace, and E. Scordato are gratefully acknowledged for collecting the behavioral data, as is A. Starling for assisting with data management. I am indebted to the staff of the Duke Lemur Center, particularly C. Williams, DVM, J. Hurley, DVM, D. Brewer, S. Combes, K. Glenn, J. Ives, and J. Taylor, for animal handling and sample collection. I am also grateful to M. Wilson, S. Lackey, and J. Hardy for their advice and endocrine work, and to two anonymous reviewers for
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