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Testicular function, social rank and personality among wild baboons
Psychoneuroendocrinology,Vol. 16, No. 4, pp. 281-293,
1991
0306- 4530/91 $3.00 + 0.00 ©1991 Pergamon Press pie
Printed in Great Britain
REVIEW TESTICULAR FUNCTION, SOCIAL RANK AND PERSONALITY AMONG WILD BABOONS ROBERT M. SAPOLSKY Department of Biological Sciences, Stanford University, Stanford, California, U.S.A., and Institute of Primate Research, National Museums of Kenya, Karen, Nairobi, Kenya (Received 16 September 1990)
INTRODUCTION PSYCHOENDOCRINOLOGISTShave had a long-standing fascination with the testicular axis; a vast literature has reported the effects of stress upon this axis. This emphasis is understandable. The axis is exquisitely sensitive to effects of both somatic and psychogenic stressors, and the neuroendocrine mechanisms by which stress suppresses the testicular axis are numerous and complex. Moreover, the phenomenon of stress-induced suppression of testicular function is of considerable relevance: Human males often suffer from psychogenic impotency, and stressinduced suppression of reproductive behavior and physiology in non-human populations represents an important challenge for animal husbandry and conservation. Since the "bottom line" of Darwinian fitness is, of course, reproduction, anything which can influence reproduction is likely to be of some evolutionary relevance. Since 1978, I have studied the effects of stress upon the testicular axis in a unique study population: wild baboons living in the Serengeti plains of East Africa. I have asked: (1) What are the circumstances and mechanisms by which stressors suppress testicular physiology in these animals? (2) How do personality and dominance rank in this primate society, as well as the type of society itself, influence the response of the testicular axis to stress? (3) What are the neuroendocrine mechanisms that mediate individual differences in testicular function? These mechanistic questions are the building blocks for studying larger issues: Why do some bodies and psyches respond to stress differently than others, and why do individuals differ in their vulnerability to stress-related disease? OLIVE BABOONS AND SOCIAL DOMINANCE These were questions I sought to answer in studying baboons. A wild population was preferable to a captive one; behavior would not be distorted by the spatial or demographic constraints unavoidable in captivity. Furthermore, animals in the wild are exposed to normal stressors and pathogens and can be followed throughout their lives. This allowed me to test whether the findings of stress physiologists in the laboratory applied to a more natural setting. Address correspondence and reprint requests to: Dr. Robert M. Sapolsky, Stanford University, Department of Biological Sciences, Herrin Laboratories, Room 3, Stanford CA 94305, USA. 281
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The olive baboon (Papio anubis) is ideal for these studies. It is intelligent, long-lived, and resides in social troops of 50-200 individuals. It is large and thus easily observed in the open grassland. Its ecosystem is rich; animals spend minimal time feeding and have few worries about predators (Strum, 1982; Smuts, 1986). Of importance, this allows baboons to devote hours each day to generating social stressors for each other, much as in our own ecologically buffered lives. Central to these social stressors is the dominance hierarchy. For the male baboons that I study, social rank is a strong predictor of quality of life; thus, my initial questions focused on the relationship between rank and testicular function. Even in the best of ecosystems, resources and social perquisites are finite, and among male baboons they are divided unevenly along lines of rank. Dominance hierarchies emerge, with rank determining ease of access to food, social grooming, resting sites and, to some extent, sexual partners. Attaining and maintaining high rank is a vastly complex task, part of the attraction of studying these animals. In part, it involves simple issues of aggression or, more often, the threat of aggression. Male baboons fight frequently, often inflicting severe or even fatal injuries. Rank can change from the outcome of a fight. Baboons also have various conventionalized gestures that threaten aggression, for example, a "threat yawn", where canines are displayed near the face of a rival, which can substitute for aggression itself. In addition, rank is determined by skill in handling socially stressful situations. For example, a male may be in a sexual consortship with an estrus female for days, attempting to maintain exclusive sexual access to her. Throughout, he may be harassed by another male, who may not overtly threaten but simply shadow so closely as to make it impossible for the first male to mate, feed or rest. Often, the first male will voluntarily relinquish the consortship. As another example, forming a cooperative coalition with another male can be very helpful in a fight; however, when the fight actually occurs, the male often fails to aid his coalitional parmer, or even defects to the opposing side. Thus, the competition for rank typically requires more than mere strength, body mass or canine length. At least as important is the ability to predict and control social circumstances, and the capacity to form cooperative affiliations and to defect from them at advantageous times. In short, social skill, a taste for game theory and the ability to endure social stress are essential. I questioned whether males succeeding in this world had stress-responses that differed from lower-ranking animals. To study this, males were observed in a manner to preclude bias (for example, in a random sequence in order to avoid observing only those doing something interesting at the time) (Altmann, 1971). Dominance hierarchies are generated from outcomes of approach-avoidance interactions: who avoids whom, who is supplanted from a resting or feeding site by whom, etc. (Packer, 1977; Strum, 1982). To obtain endocrine data, animals are anesthetized with the dissociative anesthetic phencyclidine, injected by a syringe fired from a blowgun. The anesthetic itself does not affect testicular function within this timespan (Sapolsky, 1982). Subjects are darted at the same time of day, to avoid circadian fluctuations in hormone values. Animals who are ill, injured, or have recently mated or had a fight are not darted, to avoid distortions of basal values. Animals cannot be aware that they are targeted for darting, in order to avoid anticipatory stress. The first blood sample must be obtained within a few minutes of the onset of the anesthetic; at that time, testosterone secretion has not yet increased in response to the stress of anesthetization, so that the first blood sample still reflects basal values.
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TESTOSTERONEt RANK AND PERSONALITY IN BABOONS
How Are Testosterone Concentrations Suppressed During Stress in Baboons? A variety of social and ecological stressors suppress circulating testosterone concentrations in these baboons. Some examples are shown in Fig. 1. In black are basal testosterone concentrations from two different baboon populations in Kenya (the Masai Mara National Reserve, and the grasslands near a town called Gilgil); levels are strikingly consistent. The stripped bars show two circumstances of suppressed testosterone concentrations. In the first, suppression occurred during a period of social instability, where dominance ranks shifted frequently and unpredictably, and where rates of fights and injuries rose markedly (Sapolsky, 1983). The next three bars show suppression in three different baboon troops in Masai Mara during the East African drought of 1984. During that season, grassland biomass decreased some 75%, and animals had to devote far more time to foraging (Sapolsky, 1986a). Uncovering the neuroendocrine mechanisms mediating these instances of testicular suppression are difficult, because of the rarity and unpredictability of droughts and social instabilities. A more readily studied stressor is the response to darting and anesthetization (Fig. 2); LH and, shortly thereafter, testosterone concentrations plummet rapidly. What mechanisms bring about this suppression? The inhibition of LH release is caused by the stress-induced release of opiates. Administration of the opiate receptor antagonist naloxone not only prevents the decline in LH secretion follow the darting, but even causes a significant elevation of LH concentrations (Fig. 3). That increase suggests that opiates play a role in tonic as well as stress-induced inhibition of LH release. In contrast, stress-induced secretion of glucocorticoids does not appear to play a role in the suppression of LH release. Blockade of glucocorticoid secretion with the steroid synthesis inhibitor metyrapone fails to prevent the decline (Fig. 3), while exogenous glucocorticoids do not suppress pituitary responsiveness to
Suppression of Testosterone Titers by Social Instability and Drought 20 15 ~o~ 10 t-
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FIG. 1: B a s a l t e s t o s t e r o n e c o n c e n t r a t i o n s in b a b o o n s of different troops living in v a i l e d social a n d ecological s e t t i n g s . All s a m p l e s were o b t a i n e d b e t w e e n 0 7 0 0 h a n d 1 0 0 0 h u n d e r c o n d i t i o n s d e s c r i b e d in t h e text. "Mara" refers to b a b o o n s living in t h e M a s a i Mara National Reserve in t h e Serengetl E c o s y s t e m of s o u t h w e s t Kenya. "Gflgil" refers to b a b o o n s living in a troop in t h e agricultural region of Rift Valley Province. Central Kenya, n e a r t h e t o w n of Gflgfl. "I'alek," "Keek." a n d "GD" refer to t h r e e different b a b o o n t r o o p s w i t h i n t h e Masai Mara. D a t a from Mara b a b o o n s in 1979--83 were derived from t h e "Keek" troop. (From Sapolsky, 1987.)
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R.M. SAPOLSKY ROLE OF STRESS-INDUCED OPIATE RELEASE IN LH SUPPRESSION
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GnRH (Sapolsky, 1985). Stress-induced activation of the sympathetic nervous system also does not appear to play a role in the suppression; administration of the sympathetic pre-ganglionic blocker chlorisondamine fails to prevent the stress-induced decline in LH concentrations (Fig. 3). Finally, despite the increase in prolactin secretion that is often observed during stress (Rose, 1985), no rise in prolactin occurs in these animals following darting stress, ruling out a role for this peptide in suppressing LH secretion. Naloxone, at the dose employed in Fig. 3, is thought to bind to all three opiate receptor types (reviewed in Sapolsky & Krey, 1988). We have shown that a lower naloxone dose commensurate with occupancy of only ~t-opiate receptors slows the stress-induced decline in LH concentrations, suggesting a role for its preferred endogenous ligand, IB-endorphin. In addition, administration of the K-receptor antagonist MR 1452 also delays the decline in LH, implicating its preferred endogenous ligand, dynorphin. This suppressive role for the opiates during stress, and the likely mediating receptor types, have been documented earlier (reviewed in Sapolsky & Krey, 1988). The suppression of LH release by opiates is actually secondary to their suppression of GnRH release from the hypothalamus. As evidence, opiates do not inhibit pituitary responsiveness to GnRH, but they do decrease hypothalamo-pituitary portal concentrations of GnRH and GnRH release from hypothalamic cultures in vitro (Ching, 1983; Rasmussen et al., 1983). While obviously it has not been possible to measure hypothalamic portal concentrations of GnRH in these baboons, parsimony suggests that the opiate action in these baboons is hypothalamic, rather than pituitary. This opiate-induced suppression of LH is not the sole route by which testosterone secretion is inhibited during stress. Following darting stress, if LH concentrations are maintained by
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naloxone administration, testosterone concentrations still plummet (Sapolsky, 1987). Stressinduced glucocorticoid release appears to play a role in this additional route of suppression. Administration of exogenous glucocorticoids to these baboons decreases LH bioactivity (Sapolsky, 1985), possibly due to glucocorticoid-induced glycosylation of the peptide, for which there is precedent (Chappel et al., 1983). The decline in bioactivity also could have been an artifact, as serum glucocorticoid concentrations could have been sufficient to directly inhibit Leydig cell function in the in vitro test of bioactivity. However, whether a real phenomenon or not, the reduction in LH bioactivity is rather small. A far stronger regulatory step is at the testes, where glucocorticoids profoundly inhibit testicular responsiveness to LH (Fig. 4). This appears to play a major role in the stress-induced suppression of testosterone secretion in these animals; there is an excellent correlation in individual baboons between how sensitive their testicular axis is to the suppressive effects of stress and how sensitive their testes are to the direct suppressive actions of glucocorticoids (Fig. 5). Numerous laboratory studies have demonstrated that glucocorticoids inhibit testicular sensitivity to LH; the best-implicated mechanism for this is a steroid-induced reduction in the number of LH receptors (Bambino & Hsueh, 1981; Johnson et al., 1982; Cumming et al., 1983). To summarize, during stress (or, at least, during darting stress), testosterone secretion declines rapidly in these baboons because of (1) inhibition of LH release by opiates (probably sec15o---o
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FIG. 5" Relationship between sensitivity to immobilization/ anesthetlzation-induced declines in testosterone ('1")concentration and glucocorticoid-induced s u p p r e s s i o n of testicular responsiveness to GnRH challenge. The X axis indicates the absolute decline of T concentrations following the 6 h r postimmobilization (i.e., time 0 T m i n u s the 6-hr T). The Y axis indicates the extent to w h i c h d e x a m e t h a s o n e (DEX) s u p pressed the rise in T concentrations after GnRH administration [absolute rise in T c o n c e n t r a t i o n 60 rain after GnRH administration in the a b s e n c e of DEX m i n u s the absolute rise at s a m e time in the p r e s e n c e of DEX). There w a s a highly significant (p<0.004) correlation between the two indices, indicating that individuals m o s t sensitive to the suppressive effects of s t r e s s on T concentrations were also m o s t sensitive to the inhibitory effects of glucocorticoids u p o n testicular responsiveness. Open circles indicate high-ranking males (upper 50 percentile), a s a s s e s s e d by approach-avoidance criteria. Unless otherwise specified, high and low r a n k in s u b s e q u e n t figures follow these criteria.
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ondary to decreased GnRH release), (2) a possible decrease in LH bioactivity by glucocorticoids, and (3) inhibition of testicular responsiveness to LH by glucocorticoids. The first and third effects are well-documented in the laboratory literature, and are of major magnitude in the baboons. Stress-induced prolactin secretion does not appear to play a role in the suppression; laboratory studies suggest that more chronic stressors are needed for this role for prolactin (Rose, 1985). In addition, glucocorticoid inhibition of pituitary responsiveness to GnRH does not appear to occur in these animals; that regulatory step has been demonstrated in female but not in male rodents (Suter & Schwartz, 1985a; 1985b). Thus, the mechanisms underlying stress-induced suppression of the testicular axes in these baboons thus fit well within the framework of current knowledge about stress endocrinology, leading to the next question: Do baboons of different dominance ranks differ in their vulnerability to stress-induced testicular suppression, and if so, by what mechanisms? Rank-Related Differences in Stress-Induced Testicular Suppression Before considering how rank effects the testicular stress-response, one can ask if there are associations between dominance rank and basal testosterone concentrations. A positive correlation between basal concentrations and rank in a newly formed all-male colony of rhesus monkeys has been reported (Rose et al., 1971). However, as will be discussed below, the associations in primates among social dominance, high basal testosterone concentrations and high levels of aggression appear to occur only in unstable social settings - - groups that are newly formed or undergoing a major reorganization or some marked demographic abnormality. In studies of mixed-sex captive groups living together for long periods, no association has been observed between social dominance and high basal testosterone concentrations (Eaton & Resko, 1974; Gordon et al., 1976). Similarly, among my baboons, during the typical situation of a stable dominance hierarchy, I have never observed a correlation between rank and basal testosterone concentrations.
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FIG. 6: R a n k - r e l a t e d v a r i a t i o n in t e s t o s t e r o n e c o n c e n t r a t i o n s following d a r t i n g a n d immobilization. Lowr a n k i n g m a l e s (open circles) s h o w e d c o n t i n u o u s d e c l i n e s in t e s t o s t e r o n e c o n c e n t r a t i o n s t h r o u g h o u t t h e period. H i g h - r a n k i n g m a l e s (closed circles) s h o w e d a t r a n s i e n t elevation of t e s t o s t e r o n e c o n c e n t r a t i o n s during t h e first p o s t - s t r e s s hour. T h e s e d a t a were t a k e n from one p a r t i c u l a r year; however, t h i s rank-related difference h a s b e e n c o n s i s t e n t l y d e m o n s t r a b l e in over a decade of study. (From Sapolsky, 1986b.)
TESTOSTERONE, RANK AND PERSONALITY IN BABOONS
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There is a striking correlation, however, between rank and the response of testosterone concentrations to darting stress. While baboons in general respond to this stressor with the prompt decline in testosterone concentrations shown in Fig. 2, the subset of dominant males (by approach-avoidance criteria) not only do not show this rapid decline, but have a transient increase in testosterone concentrations (Fig. 6). How does this rank-related difference occur? It is not at the pituitary level or higher;, the decline in LH concentrations following darting is rapid and equal in both high- and low-ranking males (Sapolsky, 1986b). Instead, there are a number of differences in testicular function. As one possibility, dominant males might secrete less glucocorticoids during stress than do subordinates, and thus have less inhibition of testicular responsiveness to LH, but this is not the case (Sapolsky, 1990). Rather, the testes of dominant males appear to be less sensitive to the suppressive effects of glucocorticoids upon LH secretion; the males on the left side of Fig. 5 are predominantly high-ranking. At present, I do not know the mechanism(s) that explain why the testes differ in responsiveness in a rank-related manner. However, I have recently performed testicular biopsies on these animals and am testing two CATECHOLAMINES STIMULATE hypotheses: (1) the testes of dominant males contain TESTOSTERONE SECRETION fewer glucocorticoid receptors, and/or (2) the testes of DURING STRESS dominant males have more of the glucocorticoid-deIN HIGH-RANKING MALES grading enzyme 11-[3-dehydrogenase (which has re3 cently been demonstrated in the testes [Mondor & Lakshmi, 1990]). 1 o Low By these hypotheses, dominant males should not have as rapid a decline in testosterone concentrations 0 during stress as do subordinates. Yet, the former actu- E -1 ally have elevated concentrations. How is this accomplished? ACTH-induced secretion of adrenal androgens does not appear to contribute to the transient w - 3 elevation, as the rise cannot be replicated with exoge- Z - 4 i , nous ACTH administration (Sapolsky, 1985). Rather, U.I - 5 0 4 8 the transient rise appears to be related to rank-related differences in sympathetic nervous system function o during stress. As mentioned earlier, neutralization of Ul the sympathetic stress response with chlorisondamine ~ . does not change the LH response to stress (Fig. 3). Nor does chlorisondamine change the testosterone response to stress in subordinate males (Fig. 7). However, blocking the sympathetic stress response "5 | [ .......... I 0 4 8 completely eliminates the transient testosterone HOURS AFTER IMMOBILIZATION increase seen in high-ranking males (Fig. 7). How can sympathetic catecholamine secretion dur- Fie. 7: l o p : testosterone concentrattons ing the early phase of the stress-response increase tes- a f t e r d a r t i n g i n d o m i n a n t mal es e i t h e r tosterone secretion? Such a phenomenon has been w i t h ( o p e n c i r c l e s ) o r w t t h o u t (closed circles) c h ] o z l s o n d a m ~ e . A d m i n i s t r a t i o n reported in rodents (Frankel & Ryan, 1981), and there is of the d r u g elimtnated t_he normal, t r anprecedent for at least two mechanisms. There is sym- sient rise i n testosterone concentrations. pathetic innervation of the parenchymal blood vessels B o t t o m : testosterone c o n c e n t r a t i o n s In s u b o r d i n a t e males w i t h or w i t h o u t ch]osupplying the testes, and catecholamines can dilate the r i s o n d a m i n e . These two g r o u p s did not vessels, increasing testicular blood flow. Thus, differ. (From Sapo]sky, t986b.)
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although systemic LH concentrations may be declining, the increased local blood flow could more than compensate. Additionally, autonomic innervation of the interstitial cells occurs in Old World primates (Hodson, 1970) and may mediate direct stimulation of steroidogenesis. Why does the sympathetic nervous system increase testosterone secretion only in dominant males? Potentially, this could be due to greater catecholamine release in such animals, and/or greater target tissue sensitivity. While no data in these baboons exist concerning the first possibility, I recently have obtained data demonstrating the latter: The higher the rank, the greater the systolic blood pressure elicited by a broad range of doses of epinephrine (Fig. 8). This suggests that dominant males increase cardiovascular tone during stress to a greater extent than do subordinates; greater testicular perfusion rates would be just one of the many interesting consequences of this. Whether blood vessels in the testicular parenchyma are also more sensitive to catecholamines in dominant males is not known. Thus, dominant males have a unique testosterone stress-response, in part due to decreased testicular sensitivity to the suppressive effects of glucocorticoids, and in part due to enhanced adrenergic sensitivity to catecholamines. Is their unique testicular response of any significance? These data suggest that, by 1 hr after the onset of a stressor, testosterone levels in dominant males have risen by approximately 50%, whereas those of subordinates have fallen by approximately 50%. Is this differences likely to be physiologically relevant? As discussed elsewhere (Sapolsky, 1987), these differences are almost certainly too small and too transient to influence reproductive physiology or behavior, or rates of aggression. Most plausibly, these differences may be reflected in muscle: While androgens are most often thought to have their classic anabolic effects on muscle tissue at puberty (stimulation of growth and increased nitrogen retention, sugar transport, and numbers and efficiency of the enzymes of intermediary metabolism), these effects can occur throughout life, and relatively rapidly (cf. Max & Toop, 1983). Thus, it is conceivable that, over the course of a sustained social stressor (for example, a consortship harassment), the higher ranking male may enter the fight that often ensues with the advantage of enhanced muscle metabolism. I am currently testing this hypothesis. Are the Rank-Related Features of Testicular Function Actually Related to Social Rank? The aforementioned results suggest that social rank is a critical and straightforward factor explaining individual differences in testicular function: Baboons have diametrically opposite responses to stress, depending on their social rank. Among complex social primates, however, it is actually far from straightforward. First, social rank changes over time. Second, the physiologic correlates of rank depend on the type of society in which the rank occurs. Finally, the physiologic correlates of rank may be more related to personality than to the rank itself. I now discuss these complexities. 1) Social ranks change over time. Among baboons, a young growing male may eventually reverse the direction of dominance with a rival; a top-ranking male may sustain an injury; or a new male may join the troop and disrupt the pattem of coalitions. Any of these can cause waves of changes in the hierarchy. This plasticity has an important consequence: Predictions about the long-term consequences of testicular differences must incorporate the changing status of these animals. The physiology documented in any given season is little more than just a "still photograph" of a very dynamic system. 2) The physiologic correlates of dominance depend on the type of society in which the dominance occurs. While there may be a consistent correlation between one's rank and testicular function, is there any causality in this correlation? For example, high-ranking males tend
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FIG. 8: R a n k - r e l a t e d differences in sensitivity of systolic blood p r e s s u r e r e s p o n s e to c a t e c h o l a m i n e s . Data were analyzed according to r a n k : a n i m a l s were categorized either a s h i g h - r a n k i n g (black; from t h e u p p e r third of t h e hierarchy), m i d d l e - r a n k i n g (stripped) or Iow-ranklng (white); t h e y were weightm a t c h e d . T h e y were injected with c h l o r i s o n d a m i n e i m m e d i a t e l y aKer a n e s t h e t i z a t i o n in order to inhibit e n d o g e n o u s c a t e c h o l a m i n e release; t h e d r u g i n d u c e d equally low b a s a l systolic blood p r e s s u r e In all g r o u p s . O n e h o u r later, b a b o o n s were injected i.v. with 10 Ixg of e p i n e p h r i n e in a single bolus, a n d blood p r e s s u r e w a s m o n i t o r e d 1 m i n later, O n e h o u r after t h a t , a similar challenge w a s given with 25 lag epinephrine; 1 h r later, with 50 lag; a n d 1 h r later, with 75 lag. At all b u t t h e lowest epin e p h r i n e concentration, t h e r e w a s a stepwise relationship b e t w e e n systolic sensitivity to e p i n e p h r i n e a n d r a n k , with g r e a t e r r e s p o n s i v e n e s s OCCUlTIng with h i g h e r rank. ( U n p u b l i s h e d observations.)
to be prime-aged, in good health and well fed. Perhaps the ability to elevate testosterone concentrations transiently during stress merely results from being prime-aged. My subsequent studies suggested that the physiology does arise from rank, but it is sensitive not only to rank but also to the social setting in which the rank occurs. Most often, there is a number 2-ranking male who is an heir apparent to number 1. In 1981, however, no male had that role. Instead, a coalition of ranks 2 - 7 formed and crippled the highest ranking male in a fight, eliminating him from social competition. The coalition then
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disintegrated; any of the remaining six males could have dominated all other males in the troop, but among them, sustained social instability ensued. Ranks changed daily, rates of fights and injuries increased, feeding and sexual consortships declined, and coalitions formed and disintegrated quickly. (In contrast, in stable seasons, ranks did not shift significantly during the three months of annual study, and within individual dyads, the dominant individual of the pair won an average of 97% of the interactions [Sapolsky, 1983]). Critically, during this social instability, the usual advantageous psychologic picture of dominance in a stable setting had disappeared; now, being in this top-ranking cohort involved highly charged unpredictability and lack of control, as well as the highest rates of aggression. Sitting precariously atop a shifting hierarchy is, psychologically, very different from sitting atop a stable one - - just consider the state of mind of a dictator as the populace storms the palace gates. During the unstable 1981 season, an opposite picture of testicular function emerged than during the stable seasons. With the instability, dominant males now had the highest basal testosterone concentrations, but they were no longer able to increase these concentrations with the onset of stress. Unique features of adrenocortical function in dominant males in stable seasons had also disappeared (Sapolsky, 1983). Similar findings emerged in studies of laboratory primates, where instability can be induced by forming new social groups. As with the wild baboons during 1981, dominant males in unstable captive groups have the highest basal testosterone concentrations and the highest rates of aggression (M. mulatta, Rose et al., 1971, 1975; M. talapoin, Eberhart & Keveme, 1979; S. sciureus, Mendoza et al., 1979, and Coe et al., 1979). With the passing of time, social relations in captive colonies stabilize, and in colonies intact for 15 months or longer, dominant males no longer were observed to have the highest basal testosterone concentrations or the highest rates of aggression (M. mulatta, Gordon et al., 1976; M.fuscata, Eaton & Resko, 1974). This has two important implications. First, the physiological correlates of rank do not cause rank; in most studies of captive primates, testosterone concentrations prior to group formation do not predict eventual rank. Second, there is no single testieular profile of dominance. Instead, it depends on the type of society in which it occurs, and a critical variable seems to be whether it is a stable or unstable society. In the latter case, overt aggression plays a major role in attaining social dominance, while in the former, covert threats of aggression, psychological intimidation and the status quo are critical in maintaining dominance. 3) The physiologic correlates of dominance may he more related to personality than to the dominance itself. Social primates are not merely dominant or subordinate, nor can they be reduced to a simple rank. These complex individuals differ in behavioral styles. Males differ as to how readily they form successful cooperative coalitions, how often they play with infants, whether they displace aggression after losing a fight, etc. The testicular axes of subordinate males are more susceptible to the suppressive effects of stress than are those of dominant males. Are there any personality styles among subordinate males that are associated with being less susceptible? To test this, we formalized some 40 different stylistic features of behavior among subordinate animals conceming their styles of social affiliation, sexual behavior, aggression, etc. The highest peak testosterone concentrations were observed among the subset of subordinate males who were, arguably, the most aggressive; these had the highest rates of fights and of displacement attacks upon females, juveniles and infants. These stylistic traits, however, did not predict how readily testosterone concentrations declined during stress. In contrast, the subordinate males in whom concentrations declined the least were the subset with the highest rates of consortships with estrus females. This is a subtle observation. Among
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dominant males, high rates of sexual consortships are achieved, in large part, by success in male-male competition. Subordinate males, in contrast, cannot compete as readily, and those who achieve the rare consortship do so through a different route. Primatologists have recently come to emphasize the role of female choice in consortship formation (Smuts, 1985), and this plays a particularly important role in the formation of the rare consortship with a low-ranking male. Typically, this reflects a highly affiliated relationship between that male and female (the term "friend" has been used here [Smuts, 1985] in a way that I think is not at all anthropomorphic). Thus, the subordinate males most buffered from the effects of stress upon their testicular axes might well be those with the most pronounced patterns of social affiliation with females (Virgin & Sapolsky, unpublished data). The full implications of this observation are not yet clear. For the moment, what is most striking is the fact that what initially seemed to be an endocrine marker of social subordinance actually marks a style of subordinance. We have reached a similar conclusion in our observation that some of the adrenocortical correlates of social dominance among these animals are, in fact, correlates of a certain style of dominance (Sapolsky & Ray, 1989). Collectively, these findings are reminiscent of the classic ones demonstrating hypercortisolism among parents of children dying of cancer (Friedman et al., 1963; Wolff et al., 1964); the magnitude of the hypercortisolism was related to the coping style of the parents, with less cortisol secretion among those with religious rationalizations about the illness, who denied the facts of the disease, or who could lose themselves in the details of managing the disease. CONCLUSION Hans Selye and his intellectual descendants who formed the first generation of stress physiologists conceived of the stress response purely in terms of the magnitude of the external stressor and the extent to which homeostatic balance was disrupted by an insult. The studies showing, for example, the linearity between the magnitude of a hemorrhage and the extent of glucocorticoid secretion (Gann, 1969) are within that intellectual tradition. Certainly, it is a challenging yet pleasing task to come to understand the stress response in these bioengineering terms. In studying my baboons, questions on that level will fill many years to come; for example, studying the effects of transient testosterone fluxes on muscle metabolism. Yet, the later personality studies suggest that the testicular stress response, and in fact stress physiology as a whole, is too rich and complex to be studied only on these mechanistic levels. An external piece of reality such as the stressfulness of social subordinance may intrude, which carries with it a certain likelihood of a particular physiological consequence. Yet, the attributes of personality and psychologic makeup which influence the perception of that stressor have a profound effect on the physiological response as well. It is on this psychoendocrine level that the study of these baboons is most satisfying - - a level which most likely will generalize to ourselves.
Acknowledgements: The studies described here were made possible by the long-standing generosity of the Harry Frank Guggenheim Foundation, and by a MacArthur Fellowship. Field assistance was supplied by Richard Kones, Francis Onchiri, Hudson Oyaro, Diane Rich, Lisa Share and Reed Sutherland.
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Altman J (1971) Observational study of behavior: sampling methods. Behaviour 39: 73-90. Bambino T, Hsueh A (1981) Direct inhibitory effect of glucocorticoids upon testicular luteinizing hormone receptors and steroidogenesis in vivo and in vitro. Endocrinology 108: 2142-2148. Chappel S, Ulloa-Aguirre A, Coutifaris C (1983) Biosynthesis and secretion of follicle-stimulating hormone. Endocr Rev 4: 179-193. Ching M (1983) Morphine suppresses the proestrus surge of GnRH in pituitary portal plasma of rats. Endocrinology 112: 2209-2214. Coe C, Mendoza S, Levine S (1979) Social status constrains the stress response in the squirrel monkey. Physiol Behav 23: 633-641. Cumming D, Quigley M, Yen S (1983) Acute suppression of circulating testosterone levels by cortisol in men. J Clin Endocrinol Metab 57: 671-679. Eaton G, Resko J (1974) Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males. Horm Behav 5: 251-263. Eberhart J, Keverne E (1979) Influences of the dominance hierarchy on LH, testosterone and prolactin in male talapoin monkeys. JEndocrino183: 42-48. Frankl A, Ryan E (1981) Testicular innervation is necessary for the response of plasma testosterone levels to acute stress. BiolReprod 24: 491-496. Friedman S, Mason J, Hamburg D (1963) Urinary 17-hydroxycorticosteroid levels in parents of children with neoplastic disease: a study of chronic psychological stress. Psychosom Med 25: 364-378. Gann D (1969) Parameters of the stimulus initiating the adrenocortical response to hemorrhage. Ann NY Acad Sci 156: 740-755. Gordon T, Rose R, Bernstein I (1976) Seasonal rhythm in plasma testosterone levels in the rhesus monkey (Macaca mulatta): a three year study. Horm Behav 7: 229-236. Hodson N (1970) The nerves of the testis, epididymis, and scrotum. In: Johnson D, Gome W, Vandermark N (Eds) The Testis, vol 1. Academic Press, New York, pp 47-68. Johnson B, Welsh T, Juniewicz P (1982) Suppression of luteinizing hormone and testosterone secretion in bulls following adrenocorticotropin hormone treatment. Biol Reprod 26: 305- 313. Max S, Toop J (1983) Androgens enhance in vivo 2-deoxyglucose uptake by rat striated muscle. Endocrinology 113: 119-126. Mendoza S, Coe C, Lowe D, Levine S (1979) The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology 3: 221-230. Mondor C, Lakshmi V (1990) Corticosteroid l l-beta-dehydrogenase of rat tissues: immunological studies. Endocrinology 126: 2435-2443. Packer C (1977) Reciprocal altruism in Papio anubis. Nature 265: 441-443. Rasmussen D, Liu J, Wolf P, Yen S (1983) Endogenous opioid regulation of gonadotropin-releasing hormone release from the human fetal hypothalamus in vitro. J Clin Endocrinol Metab 57: 881-887. Rose R (1985) Psychoendocrinology. In: Wilson J, Foster D (Eds) Textbook of Endocrinology, 7th ed. Saunders, Philadelphia PA, pp 653-681. Rose R, Holaday J, Bernstein I (1971) Plasma testosterone, rank and aggressive behavior in male rhesus monkeys. Nature 231: 366-369. Rose R, Bernstein I, Gordon T (1975) Consequences of social conflict on plasma testosterone levels in rhesus monkeys. Psychosom Med 37: 50-58. Sapolsky R (1982) The endocrine stress-response and social status in the wild baboon. Horm Behav 15: 279-285. Sapolsky R (1983) Endocrine aspects of social instability in the olive baboon. Am J Primatol 5: 365-372. Sapolsky R (1985) Stress-induced suppression of testicular function in the wild baboon: role of glucocorticoids. Endocrinology 116: 2273-2279. Sapolsky R (1986a) Endocrine and behavioral correlates of drought in the wild baboon. Am J Primatol 11: 217-224. Sapolsky R (1986b) Stress-induced elevation of testosterone concentrations in high-ranking baboons: role of catecholamines. Endocrinology 118:1630-1636. Sapolsky R (1987) Stress, social status, and reproductive physiology in free-living baboons. In: Crews D (Ed) Psychobiology of Reproductive Behavior. Prentice Hall, Englewood Cliffs NJ, pp 291-322.
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Sapolsky R (1990) Adrenocortical function, social rank and personality among wild baboons. Biol Psychiatry 28: 862-874. Sapolsky R, Krey L (1988) Stress-induced suppression of luteinizing hormone concentrations in wild baboons: role of opiates. J Clin Endocrinol Metab 66: 722-726. Sapolsky R, Ray J (1989) Styles of dominance and their physiological correlates among wild baboons. Am J Primato118: 1-9. Smuts B (1985) Sex and Friendship in Baboons. Aldine Press, Hawthorne. Strum S (1982) Agonistic dominance in male baboons: an alternative view. lntJPrimatol 3: 175-189. Suter D, Schwartz N (1985a) Effects of glucocorticoids on secretion of luteinizing hormone and follicle-stimulating hormone by male rat pituitary cells in vitro. Endocrinology 117: 855-859. Suter D, Schwartz N (1985b) Effects of glucocorticoids on secretion of luteinizing hormone and follicle-stimulating hormone by female rat pituitary cells in vitro. Endocrinology 117: 849-854. Wolff C, Friedman S, Hofer M, Mason J (1964) Relationship between psychological defenses and mean urinary 17-hydroxycorticosteroidexcretion rates. Psychosom Med 26- 576-588.
1991
0306- 4530/91 $3.00 + 0.00 ©1991 Pergamon Press pie
Printed in Great Britain
REVIEW TESTICULAR FUNCTION, SOCIAL RANK AND PERSONALITY AMONG WILD BABOONS ROBERT M. SAPOLSKY Department of Biological Sciences, Stanford University, Stanford, California, U.S.A., and Institute of Primate Research, National Museums of Kenya, Karen, Nairobi, Kenya (Received 16 September 1990)
INTRODUCTION PSYCHOENDOCRINOLOGISTShave had a long-standing fascination with the testicular axis; a vast literature has reported the effects of stress upon this axis. This emphasis is understandable. The axis is exquisitely sensitive to effects of both somatic and psychogenic stressors, and the neuroendocrine mechanisms by which stress suppresses the testicular axis are numerous and complex. Moreover, the phenomenon of stress-induced suppression of testicular function is of considerable relevance: Human males often suffer from psychogenic impotency, and stressinduced suppression of reproductive behavior and physiology in non-human populations represents an important challenge for animal husbandry and conservation. Since the "bottom line" of Darwinian fitness is, of course, reproduction, anything which can influence reproduction is likely to be of some evolutionary relevance. Since 1978, I have studied the effects of stress upon the testicular axis in a unique study population: wild baboons living in the Serengeti plains of East Africa. I have asked: (1) What are the circumstances and mechanisms by which stressors suppress testicular physiology in these animals? (2) How do personality and dominance rank in this primate society, as well as the type of society itself, influence the response of the testicular axis to stress? (3) What are the neuroendocrine mechanisms that mediate individual differences in testicular function? These mechanistic questions are the building blocks for studying larger issues: Why do some bodies and psyches respond to stress differently than others, and why do individuals differ in their vulnerability to stress-related disease? OLIVE BABOONS AND SOCIAL DOMINANCE These were questions I sought to answer in studying baboons. A wild population was preferable to a captive one; behavior would not be distorted by the spatial or demographic constraints unavoidable in captivity. Furthermore, animals in the wild are exposed to normal stressors and pathogens and can be followed throughout their lives. This allowed me to test whether the findings of stress physiologists in the laboratory applied to a more natural setting. Address correspondence and reprint requests to: Dr. Robert M. Sapolsky, Stanford University, Department of Biological Sciences, Herrin Laboratories, Room 3, Stanford CA 94305, USA. 281
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The olive baboon (Papio anubis) is ideal for these studies. It is intelligent, long-lived, and resides in social troops of 50-200 individuals. It is large and thus easily observed in the open grassland. Its ecosystem is rich; animals spend minimal time feeding and have few worries about predators (Strum, 1982; Smuts, 1986). Of importance, this allows baboons to devote hours each day to generating social stressors for each other, much as in our own ecologically buffered lives. Central to these social stressors is the dominance hierarchy. For the male baboons that I study, social rank is a strong predictor of quality of life; thus, my initial questions focused on the relationship between rank and testicular function. Even in the best of ecosystems, resources and social perquisites are finite, and among male baboons they are divided unevenly along lines of rank. Dominance hierarchies emerge, with rank determining ease of access to food, social grooming, resting sites and, to some extent, sexual partners. Attaining and maintaining high rank is a vastly complex task, part of the attraction of studying these animals. In part, it involves simple issues of aggression or, more often, the threat of aggression. Male baboons fight frequently, often inflicting severe or even fatal injuries. Rank can change from the outcome of a fight. Baboons also have various conventionalized gestures that threaten aggression, for example, a "threat yawn", where canines are displayed near the face of a rival, which can substitute for aggression itself. In addition, rank is determined by skill in handling socially stressful situations. For example, a male may be in a sexual consortship with an estrus female for days, attempting to maintain exclusive sexual access to her. Throughout, he may be harassed by another male, who may not overtly threaten but simply shadow so closely as to make it impossible for the first male to mate, feed or rest. Often, the first male will voluntarily relinquish the consortship. As another example, forming a cooperative coalition with another male can be very helpful in a fight; however, when the fight actually occurs, the male often fails to aid his coalitional parmer, or even defects to the opposing side. Thus, the competition for rank typically requires more than mere strength, body mass or canine length. At least as important is the ability to predict and control social circumstances, and the capacity to form cooperative affiliations and to defect from them at advantageous times. In short, social skill, a taste for game theory and the ability to endure social stress are essential. I questioned whether males succeeding in this world had stress-responses that differed from lower-ranking animals. To study this, males were observed in a manner to preclude bias (for example, in a random sequence in order to avoid observing only those doing something interesting at the time) (Altmann, 1971). Dominance hierarchies are generated from outcomes of approach-avoidance interactions: who avoids whom, who is supplanted from a resting or feeding site by whom, etc. (Packer, 1977; Strum, 1982). To obtain endocrine data, animals are anesthetized with the dissociative anesthetic phencyclidine, injected by a syringe fired from a blowgun. The anesthetic itself does not affect testicular function within this timespan (Sapolsky, 1982). Subjects are darted at the same time of day, to avoid circadian fluctuations in hormone values. Animals who are ill, injured, or have recently mated or had a fight are not darted, to avoid distortions of basal values. Animals cannot be aware that they are targeted for darting, in order to avoid anticipatory stress. The first blood sample must be obtained within a few minutes of the onset of the anesthetic; at that time, testosterone secretion has not yet increased in response to the stress of anesthetization, so that the first blood sample still reflects basal values.
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How Are Testosterone Concentrations Suppressed During Stress in Baboons? A variety of social and ecological stressors suppress circulating testosterone concentrations in these baboons. Some examples are shown in Fig. 1. In black are basal testosterone concentrations from two different baboon populations in Kenya (the Masai Mara National Reserve, and the grasslands near a town called Gilgil); levels are strikingly consistent. The stripped bars show two circumstances of suppressed testosterone concentrations. In the first, suppression occurred during a period of social instability, where dominance ranks shifted frequently and unpredictably, and where rates of fights and injuries rose markedly (Sapolsky, 1983). The next three bars show suppression in three different baboon troops in Masai Mara during the East African drought of 1984. During that season, grassland biomass decreased some 75%, and animals had to devote far more time to foraging (Sapolsky, 1986a). Uncovering the neuroendocrine mechanisms mediating these instances of testicular suppression are difficult, because of the rarity and unpredictability of droughts and social instabilities. A more readily studied stressor is the response to darting and anesthetization (Fig. 2); LH and, shortly thereafter, testosterone concentrations plummet rapidly. What mechanisms bring about this suppression? The inhibition of LH release is caused by the stress-induced release of opiates. Administration of the opiate receptor antagonist naloxone not only prevents the decline in LH secretion follow the darting, but even causes a significant elevation of LH concentrations (Fig. 3). That increase suggests that opiates play a role in tonic as well as stress-induced inhibition of LH release. In contrast, stress-induced secretion of glucocorticoids does not appear to play a role in the suppression of LH release. Blockade of glucocorticoid secretion with the steroid synthesis inhibitor metyrapone fails to prevent the decline (Fig. 3), while exogenous glucocorticoids do not suppress pituitary responsiveness to
Suppression of Testosterone Titers by Social Instability and Drought 20 15 ~o~ 10 t-
MARA MARA MAFIA GILGIL MARA GILGIL 1979 1 9 8 0 1 9 8 2 1 9 8 2 1 9 8 3 1983
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FIG. 1: B a s a l t e s t o s t e r o n e c o n c e n t r a t i o n s in b a b o o n s of different troops living in v a i l e d social a n d ecological s e t t i n g s . All s a m p l e s were o b t a i n e d b e t w e e n 0 7 0 0 h a n d 1 0 0 0 h u n d e r c o n d i t i o n s d e s c r i b e d in t h e text. "Mara" refers to b a b o o n s living in t h e M a s a i Mara National Reserve in t h e Serengetl E c o s y s t e m of s o u t h w e s t Kenya. "Gflgil" refers to b a b o o n s living in a troop in t h e agricultural region of Rift Valley Province. Central Kenya, n e a r t h e t o w n of Gflgfl. "I'alek," "Keek." a n d "GD" refer to t h r e e different b a b o o n t r o o p s w i t h i n t h e Masai Mara. D a t a from Mara b a b o o n s in 1979--83 were derived from t h e "Keek" troop. (From Sapolsky, 1987.)
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R.M. SAPOLSKY ROLE OF STRESS-INDUCED OPIATE RELEASE IN LH SUPPRESSION
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FIG. 3 (right): Effects of naloxone (NALOX), chlorisondamlne (CHLOR), a n d metyrapone (METYR) on serum LH responses (expressed as a percentage of t h e time zero value) to a n e s t h e t i z a t i o n stress. (From Sapolsky & Krey, 1988.)
GnRH (Sapolsky, 1985). Stress-induced activation of the sympathetic nervous system also does not appear to play a role in the suppression; administration of the sympathetic pre-ganglionic blocker chlorisondamine fails to prevent the stress-induced decline in LH concentrations (Fig. 3). Finally, despite the increase in prolactin secretion that is often observed during stress (Rose, 1985), no rise in prolactin occurs in these animals following darting stress, ruling out a role for this peptide in suppressing LH secretion. Naloxone, at the dose employed in Fig. 3, is thought to bind to all three opiate receptor types (reviewed in Sapolsky & Krey, 1988). We have shown that a lower naloxone dose commensurate with occupancy of only ~t-opiate receptors slows the stress-induced decline in LH concentrations, suggesting a role for its preferred endogenous ligand, IB-endorphin. In addition, administration of the K-receptor antagonist MR 1452 also delays the decline in LH, implicating its preferred endogenous ligand, dynorphin. This suppressive role for the opiates during stress, and the likely mediating receptor types, have been documented earlier (reviewed in Sapolsky & Krey, 1988). The suppression of LH release by opiates is actually secondary to their suppression of GnRH release from the hypothalamus. As evidence, opiates do not inhibit pituitary responsiveness to GnRH, but they do decrease hypothalamo-pituitary portal concentrations of GnRH and GnRH release from hypothalamic cultures in vitro (Ching, 1983; Rasmussen et al., 1983). While obviously it has not been possible to measure hypothalamic portal concentrations of GnRH in these baboons, parsimony suggests that the opiate action in these baboons is hypothalamic, rather than pituitary. This opiate-induced suppression of LH is not the sole route by which testosterone secretion is inhibited during stress. Following darting stress, if LH concentrations are maintained by
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naloxone administration, testosterone concentrations still plummet (Sapolsky, 1987). Stressinduced glucocorticoid release appears to play a role in this additional route of suppression. Administration of exogenous glucocorticoids to these baboons decreases LH bioactivity (Sapolsky, 1985), possibly due to glucocorticoid-induced glycosylation of the peptide, for which there is precedent (Chappel et al., 1983). The decline in bioactivity also could have been an artifact, as serum glucocorticoid concentrations could have been sufficient to directly inhibit Leydig cell function in the in vitro test of bioactivity. However, whether a real phenomenon or not, the reduction in LH bioactivity is rather small. A far stronger regulatory step is at the testes, where glucocorticoids profoundly inhibit testicular responsiveness to LH (Fig. 4). This appears to play a major role in the stress-induced suppression of testosterone secretion in these animals; there is an excellent correlation in individual baboons between how sensitive their testicular axis is to the suppressive effects of stress and how sensitive their testes are to the direct suppressive actions of glucocorticoids (Fig. 5). Numerous laboratory studies have demonstrated that glucocorticoids inhibit testicular sensitivity to LH; the best-implicated mechanism for this is a steroid-induced reduction in the number of LH receptors (Bambino & Hsueh, 1981; Johnson et al., 1982; Cumming et al., 1983). To summarize, during stress (or, at least, during darting stress), testosterone secretion declines rapidly in these baboons because of (1) inhibition of LH release by opiates (probably sec15o---o
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FIG. 5" Relationship between sensitivity to immobilization/ anesthetlzation-induced declines in testosterone ('1")concentration and glucocorticoid-induced s u p p r e s s i o n of testicular responsiveness to GnRH challenge. The X axis indicates the absolute decline of T concentrations following the 6 h r postimmobilization (i.e., time 0 T m i n u s the 6-hr T). The Y axis indicates the extent to w h i c h d e x a m e t h a s o n e (DEX) s u p pressed the rise in T concentrations after GnRH administration [absolute rise in T c o n c e n t r a t i o n 60 rain after GnRH administration in the a b s e n c e of DEX m i n u s the absolute rise at s a m e time in the p r e s e n c e of DEX). There w a s a highly significant (p<0.004) correlation between the two indices, indicating that individuals m o s t sensitive to the suppressive effects of s t r e s s on T concentrations were also m o s t sensitive to the inhibitory effects of glucocorticoids u p o n testicular responsiveness. Open circles indicate high-ranking males (upper 50 percentile), a s a s s e s s e d by approach-avoidance criteria. Unless otherwise specified, high and low r a n k in s u b s e q u e n t figures follow these criteria.
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ondary to decreased GnRH release), (2) a possible decrease in LH bioactivity by glucocorticoids, and (3) inhibition of testicular responsiveness to LH by glucocorticoids. The first and third effects are well-documented in the laboratory literature, and are of major magnitude in the baboons. Stress-induced prolactin secretion does not appear to play a role in the suppression; laboratory studies suggest that more chronic stressors are needed for this role for prolactin (Rose, 1985). In addition, glucocorticoid inhibition of pituitary responsiveness to GnRH does not appear to occur in these animals; that regulatory step has been demonstrated in female but not in male rodents (Suter & Schwartz, 1985a; 1985b). Thus, the mechanisms underlying stress-induced suppression of the testicular axes in these baboons thus fit well within the framework of current knowledge about stress endocrinology, leading to the next question: Do baboons of different dominance ranks differ in their vulnerability to stress-induced testicular suppression, and if so, by what mechanisms? Rank-Related Differences in Stress-Induced Testicular Suppression Before considering how rank effects the testicular stress-response, one can ask if there are associations between dominance rank and basal testosterone concentrations. A positive correlation between basal concentrations and rank in a newly formed all-male colony of rhesus monkeys has been reported (Rose et al., 1971). However, as will be discussed below, the associations in primates among social dominance, high basal testosterone concentrations and high levels of aggression appear to occur only in unstable social settings - - groups that are newly formed or undergoing a major reorganization or some marked demographic abnormality. In studies of mixed-sex captive groups living together for long periods, no association has been observed between social dominance and high basal testosterone concentrations (Eaton & Resko, 1974; Gordon et al., 1976). Similarly, among my baboons, during the typical situation of a stable dominance hierarchy, I have never observed a correlation between rank and basal testosterone concentrations.
• High 0 Low E6
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H O U R S AFTER MOBILIZATION
FIG. 6: R a n k - r e l a t e d v a r i a t i o n in t e s t o s t e r o n e c o n c e n t r a t i o n s following d a r t i n g a n d immobilization. Lowr a n k i n g m a l e s (open circles) s h o w e d c o n t i n u o u s d e c l i n e s in t e s t o s t e r o n e c o n c e n t r a t i o n s t h r o u g h o u t t h e period. H i g h - r a n k i n g m a l e s (closed circles) s h o w e d a t r a n s i e n t elevation of t e s t o s t e r o n e c o n c e n t r a t i o n s during t h e first p o s t - s t r e s s hour. T h e s e d a t a were t a k e n from one p a r t i c u l a r year; however, t h i s rank-related difference h a s b e e n c o n s i s t e n t l y d e m o n s t r a b l e in over a decade of study. (From Sapolsky, 1986b.)
TESTOSTERONE, RANK AND PERSONALITY IN BABOONS
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There is a striking correlation, however, between rank and the response of testosterone concentrations to darting stress. While baboons in general respond to this stressor with the prompt decline in testosterone concentrations shown in Fig. 2, the subset of dominant males (by approach-avoidance criteria) not only do not show this rapid decline, but have a transient increase in testosterone concentrations (Fig. 6). How does this rank-related difference occur? It is not at the pituitary level or higher;, the decline in LH concentrations following darting is rapid and equal in both high- and low-ranking males (Sapolsky, 1986b). Instead, there are a number of differences in testicular function. As one possibility, dominant males might secrete less glucocorticoids during stress than do subordinates, and thus have less inhibition of testicular responsiveness to LH, but this is not the case (Sapolsky, 1990). Rather, the testes of dominant males appear to be less sensitive to the suppressive effects of glucocorticoids upon LH secretion; the males on the left side of Fig. 5 are predominantly high-ranking. At present, I do not know the mechanism(s) that explain why the testes differ in responsiveness in a rank-related manner. However, I have recently performed testicular biopsies on these animals and am testing two CATECHOLAMINES STIMULATE hypotheses: (1) the testes of dominant males contain TESTOSTERONE SECRETION fewer glucocorticoid receptors, and/or (2) the testes of DURING STRESS dominant males have more of the glucocorticoid-deIN HIGH-RANKING MALES grading enzyme 11-[3-dehydrogenase (which has re3 cently been demonstrated in the testes [Mondor & Lakshmi, 1990]). 1 o Low By these hypotheses, dominant males should not have as rapid a decline in testosterone concentrations 0 during stress as do subordinates. Yet, the former actu- E -1 ally have elevated concentrations. How is this accomplished? ACTH-induced secretion of adrenal androgens does not appear to contribute to the transient w - 3 elevation, as the rise cannot be replicated with exoge- Z - 4 i , nous ACTH administration (Sapolsky, 1985). Rather, U.I - 5 0 4 8 the transient rise appears to be related to rank-related differences in sympathetic nervous system function o during stress. As mentioned earlier, neutralization of Ul the sympathetic stress response with chlorisondamine ~ . does not change the LH response to stress (Fig. 3). Nor does chlorisondamine change the testosterone response to stress in subordinate males (Fig. 7). However, blocking the sympathetic stress response "5 | [ .......... I 0 4 8 completely eliminates the transient testosterone HOURS AFTER IMMOBILIZATION increase seen in high-ranking males (Fig. 7). How can sympathetic catecholamine secretion dur- Fie. 7: l o p : testosterone concentrattons ing the early phase of the stress-response increase tes- a f t e r d a r t i n g i n d o m i n a n t mal es e i t h e r tosterone secretion? Such a phenomenon has been w i t h ( o p e n c i r c l e s ) o r w t t h o u t (closed circles) c h ] o z l s o n d a m ~ e . A d m i n i s t r a t i o n reported in rodents (Frankel & Ryan, 1981), and there is of the d r u g elimtnated t_he normal, t r anprecedent for at least two mechanisms. There is sym- sient rise i n testosterone concentrations. pathetic innervation of the parenchymal blood vessels B o t t o m : testosterone c o n c e n t r a t i o n s In s u b o r d i n a t e males w i t h or w i t h o u t ch]osupplying the testes, and catecholamines can dilate the r i s o n d a m i n e . These two g r o u p s did not vessels, increasing testicular blood flow. Thus, differ. (From Sapo]sky, t986b.)
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although systemic LH concentrations may be declining, the increased local blood flow could more than compensate. Additionally, autonomic innervation of the interstitial cells occurs in Old World primates (Hodson, 1970) and may mediate direct stimulation of steroidogenesis. Why does the sympathetic nervous system increase testosterone secretion only in dominant males? Potentially, this could be due to greater catecholamine release in such animals, and/or greater target tissue sensitivity. While no data in these baboons exist concerning the first possibility, I recently have obtained data demonstrating the latter: The higher the rank, the greater the systolic blood pressure elicited by a broad range of doses of epinephrine (Fig. 8). This suggests that dominant males increase cardiovascular tone during stress to a greater extent than do subordinates; greater testicular perfusion rates would be just one of the many interesting consequences of this. Whether blood vessels in the testicular parenchyma are also more sensitive to catecholamines in dominant males is not known. Thus, dominant males have a unique testosterone stress-response, in part due to decreased testicular sensitivity to the suppressive effects of glucocorticoids, and in part due to enhanced adrenergic sensitivity to catecholamines. Is their unique testicular response of any significance? These data suggest that, by 1 hr after the onset of a stressor, testosterone levels in dominant males have risen by approximately 50%, whereas those of subordinates have fallen by approximately 50%. Is this differences likely to be physiologically relevant? As discussed elsewhere (Sapolsky, 1987), these differences are almost certainly too small and too transient to influence reproductive physiology or behavior, or rates of aggression. Most plausibly, these differences may be reflected in muscle: While androgens are most often thought to have their classic anabolic effects on muscle tissue at puberty (stimulation of growth and increased nitrogen retention, sugar transport, and numbers and efficiency of the enzymes of intermediary metabolism), these effects can occur throughout life, and relatively rapidly (cf. Max & Toop, 1983). Thus, it is conceivable that, over the course of a sustained social stressor (for example, a consortship harassment), the higher ranking male may enter the fight that often ensues with the advantage of enhanced muscle metabolism. I am currently testing this hypothesis. Are the Rank-Related Features of Testicular Function Actually Related to Social Rank? The aforementioned results suggest that social rank is a critical and straightforward factor explaining individual differences in testicular function: Baboons have diametrically opposite responses to stress, depending on their social rank. Among complex social primates, however, it is actually far from straightforward. First, social rank changes over time. Second, the physiologic correlates of rank depend on the type of society in which the rank occurs. Finally, the physiologic correlates of rank may be more related to personality than to the rank itself. I now discuss these complexities. 1) Social ranks change over time. Among baboons, a young growing male may eventually reverse the direction of dominance with a rival; a top-ranking male may sustain an injury; or a new male may join the troop and disrupt the pattem of coalitions. Any of these can cause waves of changes in the hierarchy. This plasticity has an important consequence: Predictions about the long-term consequences of testicular differences must incorporate the changing status of these animals. The physiology documented in any given season is little more than just a "still photograph" of a very dynamic system. 2) The physiologic correlates of dominance depend on the type of society in which the dominance occurs. While there may be a consistent correlation between one's rank and testicular function, is there any causality in this correlation? For example, high-ranking males tend
TESTOSTERONE, RANK AND PERSONALITY IN BABOONS 300"
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FIG. 8: R a n k - r e l a t e d differences in sensitivity of systolic blood p r e s s u r e r e s p o n s e to c a t e c h o l a m i n e s . Data were analyzed according to r a n k : a n i m a l s were categorized either a s h i g h - r a n k i n g (black; from t h e u p p e r third of t h e hierarchy), m i d d l e - r a n k i n g (stripped) or Iow-ranklng (white); t h e y were weightm a t c h e d . T h e y were injected with c h l o r i s o n d a m i n e i m m e d i a t e l y aKer a n e s t h e t i z a t i o n in order to inhibit e n d o g e n o u s c a t e c h o l a m i n e release; t h e d r u g i n d u c e d equally low b a s a l systolic blood p r e s s u r e In all g r o u p s . O n e h o u r later, b a b o o n s were injected i.v. with 10 Ixg of e p i n e p h r i n e in a single bolus, a n d blood p r e s s u r e w a s m o n i t o r e d 1 m i n later, O n e h o u r after t h a t , a similar challenge w a s given with 25 lag epinephrine; 1 h r later, with 50 lag; a n d 1 h r later, with 75 lag. At all b u t t h e lowest epin e p h r i n e concentration, t h e r e w a s a stepwise relationship b e t w e e n systolic sensitivity to e p i n e p h r i n e a n d r a n k , with g r e a t e r r e s p o n s i v e n e s s OCCUlTIng with h i g h e r rank. ( U n p u b l i s h e d observations.)
to be prime-aged, in good health and well fed. Perhaps the ability to elevate testosterone concentrations transiently during stress merely results from being prime-aged. My subsequent studies suggested that the physiology does arise from rank, but it is sensitive not only to rank but also to the social setting in which the rank occurs. Most often, there is a number 2-ranking male who is an heir apparent to number 1. In 1981, however, no male had that role. Instead, a coalition of ranks 2 - 7 formed and crippled the highest ranking male in a fight, eliminating him from social competition. The coalition then
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disintegrated; any of the remaining six males could have dominated all other males in the troop, but among them, sustained social instability ensued. Ranks changed daily, rates of fights and injuries increased, feeding and sexual consortships declined, and coalitions formed and disintegrated quickly. (In contrast, in stable seasons, ranks did not shift significantly during the three months of annual study, and within individual dyads, the dominant individual of the pair won an average of 97% of the interactions [Sapolsky, 1983]). Critically, during this social instability, the usual advantageous psychologic picture of dominance in a stable setting had disappeared; now, being in this top-ranking cohort involved highly charged unpredictability and lack of control, as well as the highest rates of aggression. Sitting precariously atop a shifting hierarchy is, psychologically, very different from sitting atop a stable one - - just consider the state of mind of a dictator as the populace storms the palace gates. During the unstable 1981 season, an opposite picture of testicular function emerged than during the stable seasons. With the instability, dominant males now had the highest basal testosterone concentrations, but they were no longer able to increase these concentrations with the onset of stress. Unique features of adrenocortical function in dominant males in stable seasons had also disappeared (Sapolsky, 1983). Similar findings emerged in studies of laboratory primates, where instability can be induced by forming new social groups. As with the wild baboons during 1981, dominant males in unstable captive groups have the highest basal testosterone concentrations and the highest rates of aggression (M. mulatta, Rose et al., 1971, 1975; M. talapoin, Eberhart & Keveme, 1979; S. sciureus, Mendoza et al., 1979, and Coe et al., 1979). With the passing of time, social relations in captive colonies stabilize, and in colonies intact for 15 months or longer, dominant males no longer were observed to have the highest basal testosterone concentrations or the highest rates of aggression (M. mulatta, Gordon et al., 1976; M.fuscata, Eaton & Resko, 1974). This has two important implications. First, the physiological correlates of rank do not cause rank; in most studies of captive primates, testosterone concentrations prior to group formation do not predict eventual rank. Second, there is no single testieular profile of dominance. Instead, it depends on the type of society in which it occurs, and a critical variable seems to be whether it is a stable or unstable society. In the latter case, overt aggression plays a major role in attaining social dominance, while in the former, covert threats of aggression, psychological intimidation and the status quo are critical in maintaining dominance. 3) The physiologic correlates of dominance may he more related to personality than to the dominance itself. Social primates are not merely dominant or subordinate, nor can they be reduced to a simple rank. These complex individuals differ in behavioral styles. Males differ as to how readily they form successful cooperative coalitions, how often they play with infants, whether they displace aggression after losing a fight, etc. The testicular axes of subordinate males are more susceptible to the suppressive effects of stress than are those of dominant males. Are there any personality styles among subordinate males that are associated with being less susceptible? To test this, we formalized some 40 different stylistic features of behavior among subordinate animals conceming their styles of social affiliation, sexual behavior, aggression, etc. The highest peak testosterone concentrations were observed among the subset of subordinate males who were, arguably, the most aggressive; these had the highest rates of fights and of displacement attacks upon females, juveniles and infants. These stylistic traits, however, did not predict how readily testosterone concentrations declined during stress. In contrast, the subordinate males in whom concentrations declined the least were the subset with the highest rates of consortships with estrus females. This is a subtle observation. Among
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dominant males, high rates of sexual consortships are achieved, in large part, by success in male-male competition. Subordinate males, in contrast, cannot compete as readily, and those who achieve the rare consortship do so through a different route. Primatologists have recently come to emphasize the role of female choice in consortship formation (Smuts, 1985), and this plays a particularly important role in the formation of the rare consortship with a low-ranking male. Typically, this reflects a highly affiliated relationship between that male and female (the term "friend" has been used here [Smuts, 1985] in a way that I think is not at all anthropomorphic). Thus, the subordinate males most buffered from the effects of stress upon their testicular axes might well be those with the most pronounced patterns of social affiliation with females (Virgin & Sapolsky, unpublished data). The full implications of this observation are not yet clear. For the moment, what is most striking is the fact that what initially seemed to be an endocrine marker of social subordinance actually marks a style of subordinance. We have reached a similar conclusion in our observation that some of the adrenocortical correlates of social dominance among these animals are, in fact, correlates of a certain style of dominance (Sapolsky & Ray, 1989). Collectively, these findings are reminiscent of the classic ones demonstrating hypercortisolism among parents of children dying of cancer (Friedman et al., 1963; Wolff et al., 1964); the magnitude of the hypercortisolism was related to the coping style of the parents, with less cortisol secretion among those with religious rationalizations about the illness, who denied the facts of the disease, or who could lose themselves in the details of managing the disease. CONCLUSION Hans Selye and his intellectual descendants who formed the first generation of stress physiologists conceived of the stress response purely in terms of the magnitude of the external stressor and the extent to which homeostatic balance was disrupted by an insult. The studies showing, for example, the linearity between the magnitude of a hemorrhage and the extent of glucocorticoid secretion (Gann, 1969) are within that intellectual tradition. Certainly, it is a challenging yet pleasing task to come to understand the stress response in these bioengineering terms. In studying my baboons, questions on that level will fill many years to come; for example, studying the effects of transient testosterone fluxes on muscle metabolism. Yet, the later personality studies suggest that the testicular stress response, and in fact stress physiology as a whole, is too rich and complex to be studied only on these mechanistic levels. An external piece of reality such as the stressfulness of social subordinance may intrude, which carries with it a certain likelihood of a particular physiological consequence. Yet, the attributes of personality and psychologic makeup which influence the perception of that stressor have a profound effect on the physiological response as well. It is on this psychoendocrine level that the study of these baboons is most satisfying - - a level which most likely will generalize to ourselves.
Acknowledgements: The studies described here were made possible by the long-standing generosity of the Harry Frank Guggenheim Foundation, and by a MacArthur Fellowship. Field assistance was supplied by Richard Kones, Francis Onchiri, Hudson Oyaro, Diane Rich, Lisa Share and Reed Sutherland.
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