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Testosterone is related to deviance in male army veterans, but relationships are not moderated by cortisol
Biological Psychology 96 (2014) 72–76
Contents lists available at ScienceDirect
Biological Psychology journal homepage: www.elsevier.com/locate/biopsycho
Testosterone is related to deviance in male army veterans, but relationships are not moderated by cortisol Allan Mazur a,∗ , Alan Booth b a b
Maxwell School, Syracuse University, Syracuse, NY, United States Department of Sociology, Pennsylvania State University, State College, PA, United States
a r t i c l e
i n f o
Article history: Received 23 July 2013 Accepted 27 November 2013 Available online 10 December 2013 Keywords: Men’s testosterone Dominance and aggression Influence of cortisol
a b s t r a c t The Vietnam Experience Study (VES) of 4462 male U.S. Army veterans is the first large dataset used to demonstrate that testosterone (but not cortisol) is correlated with diverse measures of antisocial, aggressive or dominant behavior. Many subsequent studies have sustained these relationships while also pointing to important caveats. Some researchers suggest that testosterone is correlated to dominance and aggression only (or mostly) in people with low cortisol, not in those with high cortisol. Here we look back to the VES to test this “dual hormone” hypothesis. We find no testosterone–cortisol interaction for seven measures of antisocial deviance. We consider scope conditions under which the dual hormone hypothesis may be valid. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Many empirical studies relate high testosterone (T) to antisocial deviance, dominance, aggression, competitiveness, and leader-like behavior (Archer, 2006; Carré, McCormick, & Hariri, 2011; Dabbs & Dabbs, 2000; Mazur and Booth, 1998), especially in men, perhaps also in women (e.g., Denson, Mehta, & Ho Tan, 2013). These high-T behaviors are theoretically coherent, all status seeking, all reflecting unusual assertiveness and confidence when facing stressful barriers, whether these are raised by individual challengers, authority figures, or organizational norms and rules. Several factors modulate the relationship between T and associated behaviors, including peer pressure and family relations (Booth, Johnson, Granger, Crouter, & McHale, 2003), personal traits and motivations (Stanton & Schultheiss, 2009), emotions (Chichinadze et al., 2012), and physiological coping response (Salvador, 2005). Here we focus on the suggestion by several researchers that the relationship is moderated by cortisol (C), the “stress hormone,” so named because it reliably elevates in stressful situations (e.g., Terburg, Morgan, & van Honk, 2009). According to the “dual hormone hypothesis,” T is related to dominance when the actor’s C is low, but not (or less, or inversely) related when C is high (e.g., Mehta & Josephs, 2010). This dual hormone hypothesis is intuitively appealing, suggesting that the people most likely to act dominantly, to break norms or otherwise scale stressful barriers, are those least
∗ Corresponding author. Tel.: +1 315 445 1970. E-mail address: [email protected] (A. Mazur). 0301-0511/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.biopsycho.2013.11.015
bothered by the stressor, thus low in C. For high-C individuals, the barrier is too intimidating to challenge. Studies on humans published to date provide some empirical support for the dual hormone hypothesis but are based on relatively small samples. Dabbs, Jurkovic, and Frady (1991) studied 113 late-adolescent incarcerated male offenders and found a stronger relationship between T and “violence” (method of measurement unspecified) in a low-C subgroup than in a high-C subgroup, but the interaction was not found for other measures of aggression. Popma et al. (2007) had 103 early-adolescent boys in a delinquency program complete the Buss-Durkee Hostility Inventory to self-report overt (i.e., acted out) and covert (not expressed openly) aggression; they found a T × C interaction explaining overt but not covert aggression. Mehta and Josephs (2010) put the dual hormone hypothesis on firmer ground with two experimental studies, one on leadership, the other on competition. One hundred college students (half women) participated in Study 1, in which pairs were formed of unacquainted subjects, one designated “leader,” the other “follower,” and asked to perform a task. Performance was videotaped so that leaders could later be rated on dominance. In both sexes, T was related to dominant leadership when C was low but not when C was high. In Study 2, 64 male college students were paired to compete on a cognitive task in which victory and defeat were experimentally manipulated. After the competition, the men were asked if they wanted to re-challenge their opponents to a second competition; an affirmative answer was counted as a dominant response. T was positively related to dominance when C was low, but negatively related to dominance when C was high.
A. Mazur, A. Booth / Biological Psychology 96 (2014) 72–76
In a recent analysis of six studies of women’s intercollegiate sports teams, with a combined sample of almost 90 women, Edwards and Castro (2013) found that T measured before a game was correlated with a woman’s status within her team, but only for those with low cortisol before the game. Ziloli and Watson (2012) had 70 male college students form pairs to play the computer game Tetris, which was rigged to randomly assign winners and losers. Winners with the pre-competition combination of high T and low C showed greater post-game T than players in other precompetition hormone combinations. T response is not a measure of dominance per se, but the result is interpretable as supporting the dual hormone hypothesis. Carré and Mehta (2011) call for research on larger samples with sufficient statistical power to detect T × C interactions. Here we test the interaction with a very large sample (n = 4462) of male army veterans, using data collected for the Vietnam Experience Study (VES). As an historical note, the VES was the first large dataset used to demonstrate substantial correlations between T and various measures of deviant behavior (Booth & Dabbs, 1993; Booth & Osgood, 1993; Dabbs & Morris, 1990; Mazur, 1995). 2. Methods 2.1. The VES sample The VES, archived by the U.S. Centers for Disease Control (1989; http://www.cdc.gov/nceh/veterans/default1c.htm), used random selection of military records to find a sample of U.S. Army enlisted men who had served in Vietnam and a comparison sample who served elsewhere. All these men entered the army for the first time during 1965–1971 and were discharged alive after serving a minimum of 16 weeks of active duty but no more than a single term of enlistment. At the time of the initial interview the men ranged in age from 30 to 47; 95% were from 33 to 42. All men had pay grades E-1 to E-5 at discharge, corresponding to noncommissioned ranks; officers were excluded. Also excluded were men whose military occupational specialty was “duty soldier” (someone likely to have had behavior or conduct problems identified during training) or “trainee” (someone who never successfully finished training in the United States). After considerable effort, 82% of these men were successfully traced, found to be alive, and interviewed by telephone. A random sample of these men was invited free of charge to the Lovelace Medical Foundation in Albuquerque, NM for two days of physical and psychological examinations in 1985–1986. A total of 4462 men (a 69% acceptance rate) took the exam. Men serving in Vietnam and elsewhere do not differ importantly on variables considered here and are combined. 2.2. Testosterone and cortisol Men typically arrived at Lovelace in the afternoon for orientation. The next morning, before eating, blood was drawn between 8 and 10 a.m. to minimize circadian variation within the sample. Total hormone concentrations were measured with standard double antibody radioimmunoassay systems (Leeco Diagnostics, Southfield, MI). Assay results were monitored for quality by randomly running “blind” duplicate measurements on 5% of the samples. In general, correlations between first and duplicate measures were high, and reliability was kept within accepted performance criteria with coefficients of variation <10%. (For details of methodology see http://www.cdc.gov/nceh/veterans/pdfs/supplements/ supplementa/laboratorymethodsandqualitycontrol1 4.pdf.) Low and high reference values for each hormone are defined by the CDC as the 5th and 95th percentiles, respectively, of all
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men taking the examination. The low and high reference values for testosterone are 348 and 1103 ng/dl (mean = 680, SD = 235, median = 657), and for cortisol are 10 and 28 g/dl (mean = 18.2, SD = 5.5, median = 17.5). The two hormones are barely correlated, with r = 0.05 (p = .002).
2.3. Deviance measures Subjects were given the Diagnostic Interview Schedule (Centers for Disease Control, 1989), a standardized questionnaire designed to assess the lifetime occurrence of certain psychiatric conditions. Closely following an earlier study of the VES (Mazur, 1995), we constructed seven indicators of antisocial behavior as follows. JUVENILE DELINQUENCY. Respondents were asked 10 questions about juvenile delinquency before age 18, including trouble in school or with the police, running away from home, lying, stealing, fighting and destroying property. Positive responses were summed and collapsed into five groups, scored 0 (=low delinquency) through 4 (high delinquency), the percentage distribution being 21%, 24%, 19%, 14% and 22%, respectively. PAY GRADE. Respondents’ final ranks at discharge ranged from private through sergeant or specialist fifth class. Ranks are equivalent to final pay grade, E1 (low) through E5. Normally men reach the top ranks/pay grades by the end of their enlistment: 39% left the army as E5s, and 49% left with grade E4. The lowest paid soldiers (E1, E2, E3), those least integrated into, or least compliant with, the army organizational structure, are combined as the most deviant group. The gamma correlation between pay grade and having gone AWOL is −0.71 (p < .0001). ALCOHOL. Respondents were asked several questions about alcohol abuse. We selected four items pertaining to trouble in a job or school because of drinking, drunk driving, being arrested while drinking, and physical fights while drinking. Respondents are scored 0 (low abuse) if they answered “no” to all questions (53%), 1 if they gave a single “yes” (24%), 2 for two affirmatives (13%), and 3 (high abuse) for three or four “yeses” (10%). DRUGS. Respondents were shown a list of drugs and asked is they had ever used any to get high or without a prescription. Those answering “yes” were then asked if this happened within the past month. Respondents were scored 0 if they had used no drugs (35%), 1 if they had but not in the past month (48%), and 2 if they had been users in the past month (17%). VIOLENCE. Respondents were asked if, as adults, they had ever hit someone hard enough so that he or she had bruises or had to stay in bed or see a doctor, they had been in more than one fight that came to swapping blows, and they had used a weapon in a fight. They were grouped by no positive response (50% of respondents), one positive response (25%), two positive responses (18%), and three positive responses (7%). VAGRANCY. Respondents were asked if they had ever traveled around for a month not knowing how long they were going to stay or where they were going to work, and if there has ever been a period when they had no regular place to live for at least a month. Respondents were scored “yes” if they gave a positive response to either question (12%), otherwise “no.” ILLICIT. Two questions were asked about law breaking (Have you ever been arrested since age 18? Have you had at least four traffic tickets?) and two about sexual adventurism (During marriage did you have sexual relations outside of marriage with at least three different people? Have you ever had sex with as many as ten different people in a single year?). Respondents were scored 0 if they answered “no” to all four questions (30%), 1 if they answered “yes” to a single question (34%), 2 if “yes” on two items (22%), and 3 if they were affirmative on three or four items (14%).
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Fig. 1. Mean testosterone as a function of juvenile delinquency, for low and high cortisol.
Fig. 3. Mean testosterone as a function of alcohol abuse, for low and high cortisol.
2.4. Analysis We use both graphical and regression techniques to test for moderating effects of C on the relationships between T and deviance. Each type of analysis complements the other. Since T is an interval variable, it is suitable to plot its mean as a function of deviance score. We show seven figures, one for each deviance measure. Six of the seven deviance measures are scored so that a positive relationship between T and deviance is shown by a graph sloping upward to the right. PAY GRADE (or final rank) is coded inversely, so for this one figure, a positive relationship between T and deviance is shown by a graph sloping upward to the left. Respondents were split into two groups at median C. In each figure, T is graphed as a function of one deviance measure, separately for high-C men and for low-C men. According to the dual hormone hypothesis, T should rise most steeply with deviance among the low-C men, less steeply (or not at all) among the high-C men. Interactions of T × C were also tested with multiple regression. Each deviance measure was regressed on the independent variables T, C, and the interaction of T × C. The interaction term (or moderator) was calculated by first centering both T and C so their means are zero, then multiplying T by C. The product T × C represents the
Fig. 2. Mean testosterone as a function of pay grade, for low and high cortisol.
Fig. 4. Mean testosterone as a function of drug abuse, for low and high cortisol.
interaction or moderator term, assuming that the regression coefficient of T is a linear function of C (Jaccard & Turrisi, 2003). From the dual hormone hypothesis, we would expect regression coefficients of the interaction terms to be significant.
Fig. 5. Mean testosterone as a function of violence, for low and high cortisol.
A. Mazur, A. Booth / Biological Psychology 96 (2014) 72–76
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Table 1 Standardized regression coefficients (ˇs) for testosterone, cortisol, and their interaction term in seven models. One deviance measure is the dependent variable in each model (n = 4462). Dependent variable
ˇ for T
ˇ for C
ˇ for T × C
JUVENILE DELINQUENCY PAY GRADE ALCOHOL DRUGS VIOLENCE VAGRANCY ILLICIT
.13** −.13** .12** .22** .10** .09** .13**
−.07** −.01 .02 −.02 −.03 .01 −.04*
−.01 .01 .00 .00 −.02 .00 .00
* **
Fig. 6. Mean testosterone as a function of vagrancy, for low and high cortisol.
Fig. 7. Mean testosterone as a function of illicit behavior, for low and high cortisol.
3. Results Seven figures follow, one for each deviance measure. All show T increasing as a function of deviance score. The critical result in each figure is seen by comparing graphs for low-C and high-C men. Generally, the two graphs are nearly the same. In no figure is T more strongly related to deviance when cortisol is low than when it is high. Checking the possibility that the dual hormone hypothesis would fare better at extreme levels of C, we reran the seven figures but now comparing the quartile of men with highest C (21.5–48.0 g/dl) versus the quartile of men with lowest C (3.7–14.2 g/dl), thus leaving out that half of the sample with middling levels of C. Results were essentially unchanged with two exceptions: mean T was less linear a function of DRUGS than it was for the whole sample (probably a consequence of cutting the sample in half), but still there was no difference between high-C and low-C men. Only in the measure of VIOLENCE did mean T of low-C men rise somewhat more steeply than that of high-C men. Overall, focusing on extreme quartiles did not fortify the dual hypothesis. A peripheral observation is that the high-C graph is slightly above the low-C graph in all seven figures. Averaging across all deviance scores in all figures, T of high-C men is 26 ng/dl higher than T of low-C men. This is a small difference compared to the range of observed T values but is striking for its consistency. The slight correlation between T and C (r = 0.05), noted above, essentially accounts
p ≤ .01 p ≤ .001.
for this main effect. Mean T for high-C men is 690 ng/dl, and for low-C men is 668 ng/dl, a difference of 22 ng/dl. The seven graphical results were checked with seven multiple regression models. Each of the seven deviance measures is the dependent variable in one of the models. Thus, there is a one-to-one correspondence between graphs and models. Independent variables in all models are T and C (both centered at zero) and their interaction term, T × C. This procedure tests whether the relationship between T and antisocial behavior is moderated significantly by individual differences in C. All regression models are highly significant because of the very large sample (p < .001), however none explains much variance, with the largest R2 = .05. These weak results are not surprising because each man’s hormones were measured on only one morning, providing a barely adequate estimate of basal levels. Stepwise entry of independent variables, first T and C, second the product T × C, shows virtually no improvement in R2 . Nonetheless, standardized regression coefficients (ˇs) for the seven models provide a consistent pattern (Table 1). Betas for T are always highly significant (p < .001) and, as expected, they are always positive except for the dependent variable PAY GRADE, which is coded inversely. Betas for C are invariably smaller in magnitude than ˇs for T; only two are significant. Most importantly, betas for the interaction term T × C barely differ from zero, and none approaches significance. Thus, regression models corroborate the graphical results that C does not moderate the relations between T and deviance. We explored whether or not the basic model was challenged by the age of the men. Men ranged in age from 31 to 46 at the time of the interviews. As T production declines with age, it is possible that older respondents are less likely to report problem behavior. If C moderated the effect of T, it may have less effect on younger than older men. No such effect was detected, though we note that the age range of the VES sample is relatively small (Figs. 1–7). 4. Discussion Cortisol did not moderate the relationships between T and deviance as measured in the VES. This finding is consistent across graphical and regression methods. Much of the literature treats empirical relationships between T, on the one hand, and various antisocial, dominant, aggressive, competitive, and leader-like behaviors on the other, as all of a kind. They are minor variations on a central theme – that T facilitates the ability and willingness to attain high status by surmounting stressful barriers whether erected by personal adversaries, institutional rules, or social norms of conformity (e.g., Dabbs & Dabbs, 2000; Mazur & Booth, 1998). If we maintain that unitary perspective, the present results are troublesome for the dual hormone hypothesis. Our data are strong, the sample is large, the deviance measures cover a range of behaviors at different periods of life, the relationships are consistent, and C is uniformly irrelevant. Most of the measures of deviance
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are self-reported, but we also have the objective measure of military rank (PAY GRADE) at discharge, which is more strongly related to T among the high-C men than the low-C men. Despite these disconfirming empirical results, we regard the dual hormone hypothesis as theoretically cogent and think it profitable to consider scope conditions within which it applies, and outside of which (as here) it does not. For this we look at important differences between the VES and those experimental studies that provide strongest support for the dual hypothesis. A person’s hormone level, measured at one point in time, partly reflects a trait (i.e., the person may generally be high or low on that hormone) and partly reflects a temporary psychophysiological state (e.g., the person may be under stress or have just won a significant victory). VES participants had their hormones measured in 1985–1986, while the deviant behaviors they reported occurred earlier, by one measure as far back as youth. VES relationships between T and deviance must therefore reflect the trait component of T, not the state that the man was in while his blood was drawn, which would only add noise to the relationships. In some studies supporting the dual hormone hypothesis, dominant behaviors and hormone levels are measured at roughly the same time, so “state” effects on hormone levels, reflecting the various stresses and expectations of the proximate situation, may be implicated in the reported relationships. We suggest as a scope condition that T × C interactions are most likely to occur when hormones are measured at about the same time as dominance measurement. Imagine how this might work in an experiment on dominance. Some subjects – for extraneous reasons independent of their trait T – feel stressed in the laboratory, which both raises their C and also inhibits them from acting dominantly in the laboratory task. Among these high-C subjects, T would not correlate with dominance in that lab setting. But for calmer (low-C) subjects, T would predict dominance on the lab task, as expected. This is the dual hormone outcome. We are not implying that the dual hormone effect is an artifact of the experimental situation. To the contrary, in real life settings, hormones are continually adjusting to changes in psychophysiological state, nearly simultaneously with dominant or deferent social interaction. It is possible that our failure to find T × C interactions is due to measurement differences between the VES and the supportive studies. The VES measured total hormone concentrations from serum, whereas all confirming studies measured hormones in saliva. Salivary levels are far lower than total levels in serum and reflect that small portion of hormone that is “free” (i.e., unbound to protein) and thought to be physiologically active. Granger, Shirtcliff, Booth, Kivlighan, & Schwartz (2004) discuss validity problems with saliva assays, noting that since hormone levels are far higher in serum than in saliva, blood contamination of saliva samples can elevate levels, potentially exaggerating the correlation between them. We cannot exclude the possibility that T × C interactions are specific to saliva measures, but we think it unlikely. Hormone measurements in the VES, taken in a medical setting, were tightly controlled in procedures and time of day when blood was drawn. Most studies reporting a T × C interaction did not have these advantages, and saliva samples were collected at varying times of day. Since T and C are higher in the morning than the afternoon, the variable time of saliva sampling may have
introduced artifacts into reported results. We suggest that the timing of saliva sampling in future studies be more strictly controlled. At a theoretical level, perhaps the deviance measures we report here – most commonly regarded as anti-social behaviors – are fundamentally different than the dominance measures used in studies that support the dual hypothesis, those being focused more on attaining high status. Several authors emphasize that high status is usually attained by routes that are not anti-social (e.g., Cheng, Tracy, Foulsham, Kingstone, & Heinrich, 2013; Mazur, 2005). On the other hand, at least one of our measures, PAY GRADE, is a direct measure of status attained in the Army. References Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319–345. Booth, A., & Dabbs, J. (1993). Testosterone and men’s marriages. Social Forces, 72, 463–477. Booth, A., & Osgood, D. (1993). The influence of testosterone on deviance in adulthood. Criminology, 31, 93–117. Booth, A., Johnson, D., Granger, D., Crouter, A., & McHale, S. (2003). Testosterone and child and adolescent adjustment: The moderating role of parent–child relationships. Developmental Psychology, 39, 85–98. Carré, J., & Mehta, P. (2011). Importance of considering testosterone–cortisol interactions in predicting human aggression and dominance. Aggressive Behavior, 37, 489–491. Carré, J., McCormick, C., & Hariri, A. (2011). The social neuroendocrinology of human aggression. Psychoneuroendocrinology, 36, 935–944. Centers for Disease Control. (1989). . Health status of Vietnam veterans (Vols. 1–4 + Supplements) Atlanta, GA: U.S. Department of Health and Human Services. Cheng, J., Tracy, J., Foulsham, T., Kingstone, T., & Heinrich, J. (2013). Two ways to the top: Evidence that dominance and prestige are distinct yet viable avenues to social rank and influence. Journal of Personality and Social Psychology, 104, 103–125. Chichinadze, K., Lazarashvili, A., Chichinadze, C., & Gachechiladze, L. (2012). Testosterone dynamics during encounter: Role of emotional factors. Journal of Comparative Physiology A, 198, 485–494. Dabbs, J., & Dabbs, M. (2000). Heroes, rogues and lovers. New York: McGraw-Hill. Dabbs, J., & Morris, R. (1990). Testosterone, social class, and antisocial behavior in a sample of 4,462 men. Psychological Science, 1, 209–211. Dabbs, J. M., Jr., Jurkovic, G. J., & Frady, R. L. (1991). Salivary testosterone and cortisol among late adolescent male offenders. Journal of Abnormal Child Psychology, 19, 469–478. Denson, T., Mehta, P., & Ho Tan, D. (2013). Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology, 38, 416–424. Edwards, D., & Castro, K. (2013). Women’s intercollegiate athletic competition: Cortisol, testosterone, and the dual-hormone hypothesis as it relates to status among teammates. Hormones and Behavior, 64, 153–160. Granger, D. A., Shirtcliff, E. A., Booth, A., Kivlighan, K. T., & Schwartz, E. B. (2004). The ‘trouble’ with salivary testosterone. Psychoneuroendocrinology, 29, 1229–1240. Jaccard, J., & Turrisi, R. (2003). Interaction effects in multiple regression (2nd ed.). London: Sage. Mazur, A. (1995). Biosocial models of deviant behavior among male army veterans. Biological Psychology, 41, 271–293. Mazur, A. (2005). Biosociology of dominance and deference. New York: Rowman & Littlefield. Mazur, A., & Booth, A. (1998). Testosterone and dominance in men. Behavioral and Brain Sciences, 21, 353–363. Mehta, P., & Josephs, R. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58, 898–906. Popma, A., Vermeire, R., Geluk, C., Rinne, T., van den Brink, W., Knol, D., et al. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61, 405–411. Salvador, A. (2005). Coping with competitive situations in humans. Neuroscience and Biobehavioral Reviews, 29, 1195–1205. Stanton, S., & Schultheiss, O. (2009). The hormonal correlates of implicit power motivation. Journal of Research on Personality, 43, 942. Terburg, D., Morgan, B., & van Honk, J. (2009). The testosterone–cortisol ratio: A hormonal marker for proneness to social aggression. International Journal of Law and Psychiatry, 32, 216–223. Ziloli, S., & Watson, N. (2012). The hidden dimension of the competition effect: Basal cortisol and basal testosterone jointly predict changes in salivary testosterone after social victory in men. Psychoneuroendocrinology, 37, 1855–1865.
Contents lists available at ScienceDirect
Biological Psychology journal homepage: www.elsevier.com/locate/biopsycho
Testosterone is related to deviance in male army veterans, but relationships are not moderated by cortisol Allan Mazur a,∗ , Alan Booth b a b
Maxwell School, Syracuse University, Syracuse, NY, United States Department of Sociology, Pennsylvania State University, State College, PA, United States
a r t i c l e
i n f o
Article history: Received 23 July 2013 Accepted 27 November 2013 Available online 10 December 2013 Keywords: Men’s testosterone Dominance and aggression Influence of cortisol
a b s t r a c t The Vietnam Experience Study (VES) of 4462 male U.S. Army veterans is the first large dataset used to demonstrate that testosterone (but not cortisol) is correlated with diverse measures of antisocial, aggressive or dominant behavior. Many subsequent studies have sustained these relationships while also pointing to important caveats. Some researchers suggest that testosterone is correlated to dominance and aggression only (or mostly) in people with low cortisol, not in those with high cortisol. Here we look back to the VES to test this “dual hormone” hypothesis. We find no testosterone–cortisol interaction for seven measures of antisocial deviance. We consider scope conditions under which the dual hormone hypothesis may be valid. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Many empirical studies relate high testosterone (T) to antisocial deviance, dominance, aggression, competitiveness, and leader-like behavior (Archer, 2006; Carré, McCormick, & Hariri, 2011; Dabbs & Dabbs, 2000; Mazur and Booth, 1998), especially in men, perhaps also in women (e.g., Denson, Mehta, & Ho Tan, 2013). These high-T behaviors are theoretically coherent, all status seeking, all reflecting unusual assertiveness and confidence when facing stressful barriers, whether these are raised by individual challengers, authority figures, or organizational norms and rules. Several factors modulate the relationship between T and associated behaviors, including peer pressure and family relations (Booth, Johnson, Granger, Crouter, & McHale, 2003), personal traits and motivations (Stanton & Schultheiss, 2009), emotions (Chichinadze et al., 2012), and physiological coping response (Salvador, 2005). Here we focus on the suggestion by several researchers that the relationship is moderated by cortisol (C), the “stress hormone,” so named because it reliably elevates in stressful situations (e.g., Terburg, Morgan, & van Honk, 2009). According to the “dual hormone hypothesis,” T is related to dominance when the actor’s C is low, but not (or less, or inversely) related when C is high (e.g., Mehta & Josephs, 2010). This dual hormone hypothesis is intuitively appealing, suggesting that the people most likely to act dominantly, to break norms or otherwise scale stressful barriers, are those least
∗ Corresponding author. Tel.: +1 315 445 1970. E-mail address: [email protected] (A. Mazur). 0301-0511/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.biopsycho.2013.11.015
bothered by the stressor, thus low in C. For high-C individuals, the barrier is too intimidating to challenge. Studies on humans published to date provide some empirical support for the dual hormone hypothesis but are based on relatively small samples. Dabbs, Jurkovic, and Frady (1991) studied 113 late-adolescent incarcerated male offenders and found a stronger relationship between T and “violence” (method of measurement unspecified) in a low-C subgroup than in a high-C subgroup, but the interaction was not found for other measures of aggression. Popma et al. (2007) had 103 early-adolescent boys in a delinquency program complete the Buss-Durkee Hostility Inventory to self-report overt (i.e., acted out) and covert (not expressed openly) aggression; they found a T × C interaction explaining overt but not covert aggression. Mehta and Josephs (2010) put the dual hormone hypothesis on firmer ground with two experimental studies, one on leadership, the other on competition. One hundred college students (half women) participated in Study 1, in which pairs were formed of unacquainted subjects, one designated “leader,” the other “follower,” and asked to perform a task. Performance was videotaped so that leaders could later be rated on dominance. In both sexes, T was related to dominant leadership when C was low but not when C was high. In Study 2, 64 male college students were paired to compete on a cognitive task in which victory and defeat were experimentally manipulated. After the competition, the men were asked if they wanted to re-challenge their opponents to a second competition; an affirmative answer was counted as a dominant response. T was positively related to dominance when C was low, but negatively related to dominance when C was high.
A. Mazur, A. Booth / Biological Psychology 96 (2014) 72–76
In a recent analysis of six studies of women’s intercollegiate sports teams, with a combined sample of almost 90 women, Edwards and Castro (2013) found that T measured before a game was correlated with a woman’s status within her team, but only for those with low cortisol before the game. Ziloli and Watson (2012) had 70 male college students form pairs to play the computer game Tetris, which was rigged to randomly assign winners and losers. Winners with the pre-competition combination of high T and low C showed greater post-game T than players in other precompetition hormone combinations. T response is not a measure of dominance per se, but the result is interpretable as supporting the dual hormone hypothesis. Carré and Mehta (2011) call for research on larger samples with sufficient statistical power to detect T × C interactions. Here we test the interaction with a very large sample (n = 4462) of male army veterans, using data collected for the Vietnam Experience Study (VES). As an historical note, the VES was the first large dataset used to demonstrate substantial correlations between T and various measures of deviant behavior (Booth & Dabbs, 1993; Booth & Osgood, 1993; Dabbs & Morris, 1990; Mazur, 1995). 2. Methods 2.1. The VES sample The VES, archived by the U.S. Centers for Disease Control (1989; http://www.cdc.gov/nceh/veterans/default1c.htm), used random selection of military records to find a sample of U.S. Army enlisted men who had served in Vietnam and a comparison sample who served elsewhere. All these men entered the army for the first time during 1965–1971 and were discharged alive after serving a minimum of 16 weeks of active duty but no more than a single term of enlistment. At the time of the initial interview the men ranged in age from 30 to 47; 95% were from 33 to 42. All men had pay grades E-1 to E-5 at discharge, corresponding to noncommissioned ranks; officers were excluded. Also excluded were men whose military occupational specialty was “duty soldier” (someone likely to have had behavior or conduct problems identified during training) or “trainee” (someone who never successfully finished training in the United States). After considerable effort, 82% of these men were successfully traced, found to be alive, and interviewed by telephone. A random sample of these men was invited free of charge to the Lovelace Medical Foundation in Albuquerque, NM for two days of physical and psychological examinations in 1985–1986. A total of 4462 men (a 69% acceptance rate) took the exam. Men serving in Vietnam and elsewhere do not differ importantly on variables considered here and are combined. 2.2. Testosterone and cortisol Men typically arrived at Lovelace in the afternoon for orientation. The next morning, before eating, blood was drawn between 8 and 10 a.m. to minimize circadian variation within the sample. Total hormone concentrations were measured with standard double antibody radioimmunoassay systems (Leeco Diagnostics, Southfield, MI). Assay results were monitored for quality by randomly running “blind” duplicate measurements on 5% of the samples. In general, correlations between first and duplicate measures were high, and reliability was kept within accepted performance criteria with coefficients of variation <10%. (For details of methodology see http://www.cdc.gov/nceh/veterans/pdfs/supplements/ supplementa/laboratorymethodsandqualitycontrol1 4.pdf.) Low and high reference values for each hormone are defined by the CDC as the 5th and 95th percentiles, respectively, of all
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men taking the examination. The low and high reference values for testosterone are 348 and 1103 ng/dl (mean = 680, SD = 235, median = 657), and for cortisol are 10 and 28 g/dl (mean = 18.2, SD = 5.5, median = 17.5). The two hormones are barely correlated, with r = 0.05 (p = .002).
2.3. Deviance measures Subjects were given the Diagnostic Interview Schedule (Centers for Disease Control, 1989), a standardized questionnaire designed to assess the lifetime occurrence of certain psychiatric conditions. Closely following an earlier study of the VES (Mazur, 1995), we constructed seven indicators of antisocial behavior as follows. JUVENILE DELINQUENCY. Respondents were asked 10 questions about juvenile delinquency before age 18, including trouble in school or with the police, running away from home, lying, stealing, fighting and destroying property. Positive responses were summed and collapsed into five groups, scored 0 (=low delinquency) through 4 (high delinquency), the percentage distribution being 21%, 24%, 19%, 14% and 22%, respectively. PAY GRADE. Respondents’ final ranks at discharge ranged from private through sergeant or specialist fifth class. Ranks are equivalent to final pay grade, E1 (low) through E5. Normally men reach the top ranks/pay grades by the end of their enlistment: 39% left the army as E5s, and 49% left with grade E4. The lowest paid soldiers (E1, E2, E3), those least integrated into, or least compliant with, the army organizational structure, are combined as the most deviant group. The gamma correlation between pay grade and having gone AWOL is −0.71 (p < .0001). ALCOHOL. Respondents were asked several questions about alcohol abuse. We selected four items pertaining to trouble in a job or school because of drinking, drunk driving, being arrested while drinking, and physical fights while drinking. Respondents are scored 0 (low abuse) if they answered “no” to all questions (53%), 1 if they gave a single “yes” (24%), 2 for two affirmatives (13%), and 3 (high abuse) for three or four “yeses” (10%). DRUGS. Respondents were shown a list of drugs and asked is they had ever used any to get high or without a prescription. Those answering “yes” were then asked if this happened within the past month. Respondents were scored 0 if they had used no drugs (35%), 1 if they had but not in the past month (48%), and 2 if they had been users in the past month (17%). VIOLENCE. Respondents were asked if, as adults, they had ever hit someone hard enough so that he or she had bruises or had to stay in bed or see a doctor, they had been in more than one fight that came to swapping blows, and they had used a weapon in a fight. They were grouped by no positive response (50% of respondents), one positive response (25%), two positive responses (18%), and three positive responses (7%). VAGRANCY. Respondents were asked if they had ever traveled around for a month not knowing how long they were going to stay or where they were going to work, and if there has ever been a period when they had no regular place to live for at least a month. Respondents were scored “yes” if they gave a positive response to either question (12%), otherwise “no.” ILLICIT. Two questions were asked about law breaking (Have you ever been arrested since age 18? Have you had at least four traffic tickets?) and two about sexual adventurism (During marriage did you have sexual relations outside of marriage with at least three different people? Have you ever had sex with as many as ten different people in a single year?). Respondents were scored 0 if they answered “no” to all four questions (30%), 1 if they answered “yes” to a single question (34%), 2 if “yes” on two items (22%), and 3 if they were affirmative on three or four items (14%).
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Fig. 1. Mean testosterone as a function of juvenile delinquency, for low and high cortisol.
Fig. 3. Mean testosterone as a function of alcohol abuse, for low and high cortisol.
2.4. Analysis We use both graphical and regression techniques to test for moderating effects of C on the relationships between T and deviance. Each type of analysis complements the other. Since T is an interval variable, it is suitable to plot its mean as a function of deviance score. We show seven figures, one for each deviance measure. Six of the seven deviance measures are scored so that a positive relationship between T and deviance is shown by a graph sloping upward to the right. PAY GRADE (or final rank) is coded inversely, so for this one figure, a positive relationship between T and deviance is shown by a graph sloping upward to the left. Respondents were split into two groups at median C. In each figure, T is graphed as a function of one deviance measure, separately for high-C men and for low-C men. According to the dual hormone hypothesis, T should rise most steeply with deviance among the low-C men, less steeply (or not at all) among the high-C men. Interactions of T × C were also tested with multiple regression. Each deviance measure was regressed on the independent variables T, C, and the interaction of T × C. The interaction term (or moderator) was calculated by first centering both T and C so their means are zero, then multiplying T by C. The product T × C represents the
Fig. 2. Mean testosterone as a function of pay grade, for low and high cortisol.
Fig. 4. Mean testosterone as a function of drug abuse, for low and high cortisol.
interaction or moderator term, assuming that the regression coefficient of T is a linear function of C (Jaccard & Turrisi, 2003). From the dual hormone hypothesis, we would expect regression coefficients of the interaction terms to be significant.
Fig. 5. Mean testosterone as a function of violence, for low and high cortisol.
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Table 1 Standardized regression coefficients (ˇs) for testosterone, cortisol, and their interaction term in seven models. One deviance measure is the dependent variable in each model (n = 4462). Dependent variable
ˇ for T
ˇ for C
ˇ for T × C
JUVENILE DELINQUENCY PAY GRADE ALCOHOL DRUGS VIOLENCE VAGRANCY ILLICIT
.13** −.13** .12** .22** .10** .09** .13**
−.07** −.01 .02 −.02 −.03 .01 −.04*
−.01 .01 .00 .00 −.02 .00 .00
* **
Fig. 6. Mean testosterone as a function of vagrancy, for low and high cortisol.
Fig. 7. Mean testosterone as a function of illicit behavior, for low and high cortisol.
3. Results Seven figures follow, one for each deviance measure. All show T increasing as a function of deviance score. The critical result in each figure is seen by comparing graphs for low-C and high-C men. Generally, the two graphs are nearly the same. In no figure is T more strongly related to deviance when cortisol is low than when it is high. Checking the possibility that the dual hormone hypothesis would fare better at extreme levels of C, we reran the seven figures but now comparing the quartile of men with highest C (21.5–48.0 g/dl) versus the quartile of men with lowest C (3.7–14.2 g/dl), thus leaving out that half of the sample with middling levels of C. Results were essentially unchanged with two exceptions: mean T was less linear a function of DRUGS than it was for the whole sample (probably a consequence of cutting the sample in half), but still there was no difference between high-C and low-C men. Only in the measure of VIOLENCE did mean T of low-C men rise somewhat more steeply than that of high-C men. Overall, focusing on extreme quartiles did not fortify the dual hypothesis. A peripheral observation is that the high-C graph is slightly above the low-C graph in all seven figures. Averaging across all deviance scores in all figures, T of high-C men is 26 ng/dl higher than T of low-C men. This is a small difference compared to the range of observed T values but is striking for its consistency. The slight correlation between T and C (r = 0.05), noted above, essentially accounts
p ≤ .01 p ≤ .001.
for this main effect. Mean T for high-C men is 690 ng/dl, and for low-C men is 668 ng/dl, a difference of 22 ng/dl. The seven graphical results were checked with seven multiple regression models. Each of the seven deviance measures is the dependent variable in one of the models. Thus, there is a one-to-one correspondence between graphs and models. Independent variables in all models are T and C (both centered at zero) and their interaction term, T × C. This procedure tests whether the relationship between T and antisocial behavior is moderated significantly by individual differences in C. All regression models are highly significant because of the very large sample (p < .001), however none explains much variance, with the largest R2 = .05. These weak results are not surprising because each man’s hormones were measured on only one morning, providing a barely adequate estimate of basal levels. Stepwise entry of independent variables, first T and C, second the product T × C, shows virtually no improvement in R2 . Nonetheless, standardized regression coefficients (ˇs) for the seven models provide a consistent pattern (Table 1). Betas for T are always highly significant (p < .001) and, as expected, they are always positive except for the dependent variable PAY GRADE, which is coded inversely. Betas for C are invariably smaller in magnitude than ˇs for T; only two are significant. Most importantly, betas for the interaction term T × C barely differ from zero, and none approaches significance. Thus, regression models corroborate the graphical results that C does not moderate the relations between T and deviance. We explored whether or not the basic model was challenged by the age of the men. Men ranged in age from 31 to 46 at the time of the interviews. As T production declines with age, it is possible that older respondents are less likely to report problem behavior. If C moderated the effect of T, it may have less effect on younger than older men. No such effect was detected, though we note that the age range of the VES sample is relatively small (Figs. 1–7). 4. Discussion Cortisol did not moderate the relationships between T and deviance as measured in the VES. This finding is consistent across graphical and regression methods. Much of the literature treats empirical relationships between T, on the one hand, and various antisocial, dominant, aggressive, competitive, and leader-like behaviors on the other, as all of a kind. They are minor variations on a central theme – that T facilitates the ability and willingness to attain high status by surmounting stressful barriers whether erected by personal adversaries, institutional rules, or social norms of conformity (e.g., Dabbs & Dabbs, 2000; Mazur & Booth, 1998). If we maintain that unitary perspective, the present results are troublesome for the dual hormone hypothesis. Our data are strong, the sample is large, the deviance measures cover a range of behaviors at different periods of life, the relationships are consistent, and C is uniformly irrelevant. Most of the measures of deviance
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are self-reported, but we also have the objective measure of military rank (PAY GRADE) at discharge, which is more strongly related to T among the high-C men than the low-C men. Despite these disconfirming empirical results, we regard the dual hormone hypothesis as theoretically cogent and think it profitable to consider scope conditions within which it applies, and outside of which (as here) it does not. For this we look at important differences between the VES and those experimental studies that provide strongest support for the dual hypothesis. A person’s hormone level, measured at one point in time, partly reflects a trait (i.e., the person may generally be high or low on that hormone) and partly reflects a temporary psychophysiological state (e.g., the person may be under stress or have just won a significant victory). VES participants had their hormones measured in 1985–1986, while the deviant behaviors they reported occurred earlier, by one measure as far back as youth. VES relationships between T and deviance must therefore reflect the trait component of T, not the state that the man was in while his blood was drawn, which would only add noise to the relationships. In some studies supporting the dual hormone hypothesis, dominant behaviors and hormone levels are measured at roughly the same time, so “state” effects on hormone levels, reflecting the various stresses and expectations of the proximate situation, may be implicated in the reported relationships. We suggest as a scope condition that T × C interactions are most likely to occur when hormones are measured at about the same time as dominance measurement. Imagine how this might work in an experiment on dominance. Some subjects – for extraneous reasons independent of their trait T – feel stressed in the laboratory, which both raises their C and also inhibits them from acting dominantly in the laboratory task. Among these high-C subjects, T would not correlate with dominance in that lab setting. But for calmer (low-C) subjects, T would predict dominance on the lab task, as expected. This is the dual hormone outcome. We are not implying that the dual hormone effect is an artifact of the experimental situation. To the contrary, in real life settings, hormones are continually adjusting to changes in psychophysiological state, nearly simultaneously with dominant or deferent social interaction. It is possible that our failure to find T × C interactions is due to measurement differences between the VES and the supportive studies. The VES measured total hormone concentrations from serum, whereas all confirming studies measured hormones in saliva. Salivary levels are far lower than total levels in serum and reflect that small portion of hormone that is “free” (i.e., unbound to protein) and thought to be physiologically active. Granger, Shirtcliff, Booth, Kivlighan, & Schwartz (2004) discuss validity problems with saliva assays, noting that since hormone levels are far higher in serum than in saliva, blood contamination of saliva samples can elevate levels, potentially exaggerating the correlation between them. We cannot exclude the possibility that T × C interactions are specific to saliva measures, but we think it unlikely. Hormone measurements in the VES, taken in a medical setting, were tightly controlled in procedures and time of day when blood was drawn. Most studies reporting a T × C interaction did not have these advantages, and saliva samples were collected at varying times of day. Since T and C are higher in the morning than the afternoon, the variable time of saliva sampling may have
introduced artifacts into reported results. We suggest that the timing of saliva sampling in future studies be more strictly controlled. At a theoretical level, perhaps the deviance measures we report here – most commonly regarded as anti-social behaviors – are fundamentally different than the dominance measures used in studies that support the dual hypothesis, those being focused more on attaining high status. Several authors emphasize that high status is usually attained by routes that are not anti-social (e.g., Cheng, Tracy, Foulsham, Kingstone, & Heinrich, 2013; Mazur, 2005). On the other hand, at least one of our measures, PAY GRADE, is a direct measure of status attained in the Army. References Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319–345. Booth, A., & Dabbs, J. (1993). Testosterone and men’s marriages. Social Forces, 72, 463–477. Booth, A., & Osgood, D. (1993). The influence of testosterone on deviance in adulthood. Criminology, 31, 93–117. Booth, A., Johnson, D., Granger, D., Crouter, A., & McHale, S. (2003). Testosterone and child and adolescent adjustment: The moderating role of parent–child relationships. Developmental Psychology, 39, 85–98. Carré, J., & Mehta, P. (2011). Importance of considering testosterone–cortisol interactions in predicting human aggression and dominance. Aggressive Behavior, 37, 489–491. Carré, J., McCormick, C., & Hariri, A. (2011). The social neuroendocrinology of human aggression. Psychoneuroendocrinology, 36, 935–944. Centers for Disease Control. (1989). . Health status of Vietnam veterans (Vols. 1–4 + Supplements) Atlanta, GA: U.S. Department of Health and Human Services. Cheng, J., Tracy, J., Foulsham, T., Kingstone, T., & Heinrich, J. (2013). Two ways to the top: Evidence that dominance and prestige are distinct yet viable avenues to social rank and influence. Journal of Personality and Social Psychology, 104, 103–125. Chichinadze, K., Lazarashvili, A., Chichinadze, C., & Gachechiladze, L. (2012). Testosterone dynamics during encounter: Role of emotional factors. Journal of Comparative Physiology A, 198, 485–494. Dabbs, J., & Dabbs, M. (2000). Heroes, rogues and lovers. New York: McGraw-Hill. Dabbs, J., & Morris, R. (1990). Testosterone, social class, and antisocial behavior in a sample of 4,462 men. Psychological Science, 1, 209–211. Dabbs, J. M., Jr., Jurkovic, G. J., & Frady, R. L. (1991). Salivary testosterone and cortisol among late adolescent male offenders. Journal of Abnormal Child Psychology, 19, 469–478. Denson, T., Mehta, P., & Ho Tan, D. (2013). Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology, 38, 416–424. Edwards, D., & Castro, K. (2013). Women’s intercollegiate athletic competition: Cortisol, testosterone, and the dual-hormone hypothesis as it relates to status among teammates. Hormones and Behavior, 64, 153–160. Granger, D. A., Shirtcliff, E. A., Booth, A., Kivlighan, K. T., & Schwartz, E. B. (2004). The ‘trouble’ with salivary testosterone. Psychoneuroendocrinology, 29, 1229–1240. Jaccard, J., & Turrisi, R. (2003). Interaction effects in multiple regression (2nd ed.). London: Sage. Mazur, A. (1995). Biosocial models of deviant behavior among male army veterans. Biological Psychology, 41, 271–293. Mazur, A. (2005). Biosociology of dominance and deference. New York: Rowman & Littlefield. Mazur, A., & Booth, A. (1998). Testosterone and dominance in men. Behavioral and Brain Sciences, 21, 353–363. Mehta, P., & Josephs, R. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58, 898–906. Popma, A., Vermeire, R., Geluk, C., Rinne, T., van den Brink, W., Knol, D., et al. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61, 405–411. Salvador, A. (2005). Coping with competitive situations in humans. Neuroscience and Biobehavioral Reviews, 29, 1195–1205. Stanton, S., & Schultheiss, O. (2009). The hormonal correlates of implicit power motivation. Journal of Research on Personality, 43, 942. Terburg, D., Morgan, B., & van Honk, J. (2009). The testosterone–cortisol ratio: A hormonal marker for proneness to social aggression. International Journal of Law and Psychiatry, 32, 216–223. Ziloli, S., & Watson, N. (2012). The hidden dimension of the competition effect: Basal cortisol and basal testosterone jointly predict changes in salivary testosterone after social victory in men. Psychoneuroendocrinology, 37, 1855–1865.