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. Author manuscript; available in PMC: 2024 Aug 1.
Published in final edited form as: Anim Behav. 2023 Jul 4;202:99–109. doi: 10.1016/j.anbehav.2023.06.004

Lean muscle mass, not aggression, mediates a link between dominance rank and testosterone in wild male chimpanzees

Jacob D Negrey a,b,c,*, Tobias Deschner d, Kevin E Langergraber a,e
PMCID: PMC10358427  NIHMSID: NIHMS1911084  PMID: 37483564

Abstract

Testosterone promotes mating effort, which involves intraspecific aggression for males of many species. Therefore, males with higher testosterone levels are often thought to be more aggressive. For mammals living in multimale groups, aggression is hypothesized to link male social status (i.e. dominance rank) and testosterone levels, given that high status predicts mating success and is acquired partly through aggressive intragroup competition. In male chimpanzees, Pan troglodytes, dominance rank has been repeatedly linked to interindividual variation in testosterone levels, but evidence directly linking interindividual variation in testosterone and aggression is lacking. In the present study, we test both aggression levels and lean muscle mass, as measured by urinary creatinine, as links between dominance rank and testosterone levels in a large sample of wild male chimpanzees. Multivariate analyses indicated that dominance rank was positively associated with total rates of intragroup aggression, average urinary testosterone levels and average urinary creatinine levels. Testosterone was positively associated with creatinine levels but negatively associated with total aggression rates. Furthermore, mediation analyses showed that testosterone levels facilitated an association between dominance rank and creatinine levels. Our results indicate that (1) adult male chimpanzees with higher average testosterone levels are often higher ranking but not more aggressive than males with lower testosterone and (2) lean muscle mass links dominance rank and testosterone levels in Ngogo males. We assert that aggression rates are insufficient to explain links between dominance rank and testosterone levels in male chimpanzees and that other social variables (e.g. male–male relationship quality) may regulate testosterone’s links to aggression.

Keywords: aggression, challenge hypothesis, chimpanzee, competition, creatinine, mating effort, muscle mass, primate, social status, testosterone

Testosterone, an androgenic steroid hormone, mediates physiological, anatomical and behavioural traits salient to male vertebrate mating effort (Hau, 2007), including spermatogenesis (Steinberger, 1971), muscle anabolism (Griggs et al., 1989) and libido (Isidori et al., 2005). Given the prominent role of aggression in the mating effort of some male vertebrates (Clutton-Brock & Huchard, 2013), testosterone has long been thought to promote aggression (Batrinos, 2012; Collias, 1944). Among the most influential formulations of this proposed relationship is the ‘challenge hypothesis’, which posits that seasonally breeding male birds secrete more testosterone during the breeding season to stimulate aggression, prevail in male–male contests and achieve greater fertility (Wingfield et al., 1990). Since its inception, the challenge hypothesis has been reformulated for various continuously breeding and group-living species to suggest that testosterone secretion increases in any context in which aggressive behaviour could increase reproductive success (Muller, 2017; Wingfield, 2017). According to this revised challenge hypothesis, more aggressive individuals should, on average, exhibit higher testosterone levels than less aggressive individuals (Muller, 2017).

The revised challenge hypothesis has been leveraged to explain links between testosterone and rank in intrasexual dominance hierarchies, especially among primates; i.e. high-ranking male primates have been hypothesized to exhibit higher testosterone because they are more aggressive (Muller, 2017). This argument is founded on three main observations. First, status-striving behaviour represents a form of mating competition, given that high-ranking males are more likely to mate and sire offspring (Altmann, 1962; Cowlishaw & Dunbar, 1991; Feldblum et al., 2014; Georgiev et al., 2015; Launhardt et al., 2001; Watts, 2022; Wroblewski et al., 2009). Second, males often deploy aggression to acquire and maintain high rank (Gesquiere et al., 2011; Muller, 2002; Surbeck et al., 2012). Third, positive associations between dominance rank and testosterone in males have been observed for many group-living primate species (Arlet et al., 2011; Gesquiere et al., 2011; Gould & Ziegler, 2007; Rose et al., 1971; Schaebs et al., 2017; Setchell et al., 2008), a relationship that has then been attributed to heightened rates of aggression among high-ranking males (Muller, 2017). Importantly, however, not all studies of free-ranging primates report a relationship between testosterone and dominance rank. Some have observed such a relationship only during periods of hierarchical instability (Higham et al., 2013; Mendonça-Furtado et al., 2014), another found evidence that testosterone predicts future rank (Beehner et al., 2006), and others have reported little to no relationship at all (Ostner et al., 2011; Rosenbaum et al., 2021; Surbeck et al., 2012). This inconsistency suggests that variation in dominance strategies (e.g. the behavioural and/or morphological investments by which high rank is attained and maintained) and/or dominance style (e.g. the degree of despotism) may determine the presence or absence of a dominance–testosterone association in a given species, population or group.

Despite frequently observed associations between dominance rank and testosterone, evidence linking aggressiveness and testosterone levels in wild and semicaptive primates is equivocal. Some studies report an association between aggression rate and testosterone only when mating females are present (Cavigelli & Pereira, 2000), others report an association only during periods of hierarchical instability (Beehner et al., 2006), and many others report no association (Arlet et al., 2011; Kalbitzer, Heistermann et al., 2015; Lynch et al., 2002; Morino, 2015; Surbeck et al., 2012). Evidence from humans is similarly ambivalent: a recent meta-analysis of human research indicated a weak positive association between testosterone level and (largely self-reported) aggressiveness, and no experimental, causal effect of testosterone on aggression (Geniole et al., 2020). Some studies even report negative relationships between baseline testosterone levels and interindividual aggression rates in humans (Buades-Rotger et al., 2016; Chen et al.ger, 2018; McIntyre, 2011; O’Connor et al., 2002; Welker et al., 2017).

Given the relative dearth of evidence linking interindividual aggression rates and testosterone in male primates, behavioural and physiological traits other than aggression plausibly link dominance rank to testosterone. For instance, elevated muscle mass is an especially important somatic investment for adult male primates, a prioritization of mating effort (Bribiescas, 2001) that largely determines success in physical competition (Lassek & Gaulin, 2009; Mitani et al., 1996). Notably, body size and mass have been found to predict male dominance rank in some primates (bearded capuchins, Sapajus libidinosus: Fragaszy et al., 2016; mountain gorillas, Gorilla beringei beringei: Wright et al., 2019; rhesus macaques, Macaca mulatta: Bercovitch & Nürnberg, 1996; southern pig-tailed macaque, Macaca nemestrina: Tokuda & Jensen, 1969) and in many other vertebrates (brown trout, Salmo trutta: Jacob et al., 2007); yellow-bellied marmots, Marmota flaviventris: Huang et al., 2011); Asian elephants, Elephas maximus: Chelliah & Sukumar, 2013). Crucially, muscle anabolism is driven by testosterone secretion, such that increased testosterone results in greater muscle mass (Bhasin et al., 2003; Bhasin et al., 2001). Therefore, high-ranking male primates may exhibit greater average testosterone levels because they have greater muscle mass, not because they are more aggressive.

Chimpanzees, Pan troglodytes, are polygynandrous breeders that form linear male dominance hierarchies (Goodall, 1986) and exhibit high levels of intraspecific aggression (Mitani, 2009a). They were among the first primates studied under the framework of the reformulated challenge hypothesis (Muller & Wrangham, 2004a). Work on dominance, aggression and testosterone in chimpanzees has thus proven influential in the study of behavioural endocrinology and primatology. Despite the influence of these studies, however, there is little to no direct evidence linking testosterone and aggression rates in adult male chimpanzees. Although variation in male chimpanzee dominance rank has often (Muehlenbein et al., 2004; Muller & Wrangham, 2004a), but not always (Sobolewski et al., 2013), shown positive associations with testosterone levels, variation in male chimpanzee aggression rates has not (Muehlenbein et al., 2004; Muller & Wrangham, 2004a). The absence of direct links between aggression rates and testosterone undermines the argument that higher levels of aggression accounts for higher levels of testosterone among high-ranking male chimpanzees. Therefore, to understand causal links between male chimpanzee dominance rank and testosterone levels, it is imperative that we investigate traits other than aggression.

In the present study, we investigated why dominance rank is associated with testosterone levels in male chimpanzees at Ngogo, Kibale National Park, Uganda, the largest habituated community of wild chimpanzees yet studied (Wood et al., 2017). We began by conceptually replicating prior work on wild chimpanzees (Muehlenbein et al., 2004; Muller & Wrangham, 2004a), testing bivariate relationships between dominance and aggression and using multivariate analyses to simultaneously test several predictors of testosterone levels, including dominance rank, urinary creatinine (a proxy for lean muscle mass) and age. We then used mediation analyses to test statistical links between dominance and testosterone. Mediation analysis assesses the proportion of a predictor’s association with an outcome variable that can be attributed to a third variable (i.e. a mediator; MacKinnon et al., 2006). We therefore used mediation analysis to determine whether a given variable (e.g. aggression rate) accounted for an association between dominance rank and testosterone in Ngogo males.

We tested two main hypotheses. Our first hypothesis (Hypothesis 1) was that dominance rank and testosterone levels are linked primarily by aggression (Fig. 1). Importantly, we did not investigate whether individual acts of aggression are related to changes in testosterone secretion. Rather, we explored whether aggressiveness, or the sum of physical acts of intraspecific aggression over an 18-month period (controlling for observation time), was related to interindividual variation in testosterone and, consequently, whether aggression linked dominance rank to testosterone in Ngogo males.

Figure 1.

Figure 1.

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We tested two competing hypotheses: that dominance rank and testosterone levels are linked by aggression rates (Hypothesis 1) or lean muscle mass (Hypothesis 2).

Our second hypothesis (Hypothesis 2) was that dominance rank and testosterone are mainly linked by lean muscle mass (Fig. 1). While direct measures of muscle mass are impractical for the study of wild great apes, lean muscle mass can be noninvasively measured using urinary creatinine excretion. Creatinine is a product of muscle catabolism that is produced and excreted at a relatively constant rate (Heymsfield et al., 1983), such that individuals with greater muscle mass excrete more creatinine per unit time (Baxmann et al., 2008). Although approximations of muscle mass in humans have traditionally relied on 24 h creatinine measurements, adjusted spot urine samples are also effective at capturing variation in muscle mass in humans (Pandhi et al., 2021). Such a method has been successfully applied to the study of chimpanzees and other nonhuman primates, capturing variation in muscle mass pertaining to development (Emery Thompson et al., 2016; Samuni et al., 2020), food availability (Bergstrom et al., 2017; O’Connell et al., 2021) and testosterone levels (Emery Thompson al., 2012). We therefore used creatinine excretion to examine whether lean muscle mass links dominance rank and testosterone in Ngogo males.

METHODS

Ethical Note

This noninvasive study of wild chimpanzees abided by all national and international regulations for the study of free-living primates. Our research protocols were approved by the Uganda Wildlife Authority and Uganda National Council for Science and Technology and received formal exemption from review by Boston University’s Institutional Animal Care and Use Committee.

Study Site and Subjects

We studied the Ngogo chimpanzee community of Kibale National Park, Uganda, from January 2016 to July 2017. At the beginning of the study period, there were approximately 204 individuals in this community. Our subjects were 34 adult males, almost all of the adult males in the group. This tally does not include one adult male who disappeared approximately 6 months into the study period nor two males who entered adulthood more than 1 year into the study. Following prior work (Goodall, 1986; Nishida et al., 2003), males were considered ‘adults’ when aged ≥16 years. With the exception of individuals born in the last 20 years, ages were estimated by both pedigree and morphological features, as recounted in greater detail previously (Wood et al., 2017).

Behavioural Data Collection

Behavioural data were collected between January 2016 and July 2017 by J.D.N., K.E.L. or an Ngogo Chimpanzee Project field assistant (Godfrey Mbabazi, Alfred Tumusiime and Ambrose Twineomujuni). During focal animal follows (Altmann, 1974), the observer noted party composition (i.e. all individuals ≤50 m of the focal; Langergraberet al., 2013) at 15 min intervals to correct for observation time. We recorded all occurrences of aggression that occurred within the observed party, noting both the aggressor(s) and recipient(s). Aggression included any act of violence directed at a conspecific, including charges, chases and attacks. We did not record untargeted charging displays (i.e. those not directed at conspecifics) as aggression because displays do not necessarily convey aggressive intent (e.g. may instead signal physical strength) and are sometimes performed in the absence of conspecifics. To determine dominance ranks, we recorded all pant grunts, which are vocalizations given unidirectionally by subordinates to dominant individuals (Goodall, 1986). In total, we collected and analysed 20 450 unique scans of party composition, 939 acts of aggression and 582 male–male pant grunts.

Calculation of Dominance Rank

Given that males organized into two clusters or neighbourhoods that rarely interacted during the study period, we calculated two dominance hierarchies, ‘Central’ and ‘West’, which contained 25 and 9 individuals, respectively. We assigned each chimpanzee to one neighbourhood only. We then used pant grunts to calculate ordinal dominance ranks from randomized Elo-ratings (Sánchez-Tójar et al., 2018) using the ‘elo_scores’ function in the package ‘aniDom’ (Farine & Sánchez-Tójar, 2017) in R version 4.0.3 (R Core Team, 2020). We calculated each male’s dominance score as his mean rank from 1000 computed hierarchies in which the temporal order of pant grunts was randomized. To assess uncertainty in computed dominance ranks, we calculated individual rank certainty using the function ‘estimate_uncertainty_by_repeatability’ with 1000 randomizations in the package ‘aniDom’ version 0.1.4 (Farine & Sánchez-Tójar, 2017). The central and western hierarchies had repeatability scores of 0.96 and 0.91, respectively, suggesting that assigned dominance ranks were robust. Following prior studies (Langergraber et al., 2017; Muller et al., 2006), ranks were normalized from 0 (lowest) to 1 (highest) based on the number of males in each hierarchy. We then analysed both hierarchies within the same models.

Calculation of Aggression Rate

We calculated aggression rates as a given individual’s total aggressive acts divided by the number of party composition scan samples in which that individual appeared during the study period.

Urine Collection

We collected urine samples opportunistically during daily focal follows of adult male chimpanzees. We pipetted urine from leaves (Deschner et al., 2003; Surbeck et al., 2012) or plastic sheets (Knott, 1997), which we then deposited in labelled collection vials. We stored samples in a thermos with ice until returning to camp, when samples were transferred to a solar-powered freezer at −20 °C. At the end of the study period, we transported samples on dry ice to the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, storing samples at −80 °C until they were analysed. A total of 349 urine samples from 34 adult males (average ± SD: 10 ± 4.4) were collected and processed for the present study.

Hormone Analyses

Urine samples were processed and analysed by J.D.N. or a laboratory technician (Róisín Murtagh and Vera Schmeling) in the Behavioral Endocrinology Lab of the Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany. We measured testosterone using liquid chromatography–tandem mass spectrometry, following a modification of the method described by HauserDeschner, et al. (2008). We performed extractions on each sample before measuring testosterone: we added an internal standard, then performed hydrolysis (following Hauser, Schulz, et al., 2008) and solvolysis using ethyl acetate and sulfuric acid. We performed liquid chromatography using a Waters ACQUITY UPLC separation module; our eluents were water (with 0.1% formic acid) and acetonitrile. We performed mass spectrometry using a Xevo TQ-S tandem quadrupole mass spectrometer (Waters, Milford, MA, U.S.A.) and determined testosterone levels from the output using MassLynx (QuanLynx-Software).

We measured creatinine by Jaffe reaction (Husdan & Rapoport, 1968), diluting samples 1:20. Intra-assay variance for high- and low-quality controls was 1.84% and 5.94%, and interassay variance was 1.18% and 2.20%, respectively (N = 23).

To correct urinary analyte values for variation in urine concentration, the specific gravity (SG) of each sample was measured with a digital refractometer (TEC, Ober-Ramstadt, Germany). Testosterone concentration in each sample was adjusted for SG following Miller et al. (2004); final values are presented in pg/μl corr. SG. To estimate muscle mass from creatinine values, we constructed linear models to generate residuals of the slope between creatinine and specific gravity (Emery Thompson et al., 2016) using the ‘lm’ function in R. This approach is a modification of an earlier method (Emery Thompson et al., 2012) that accommodates smaller sample sizes. A linear model with specific gravity and its quadratic transformation yielded an R2adj of 0.86 (F2, 290 = 931.3, P < 0.0001). We excluded samples collected from chimpanzees exhibiting clinical signs of illness or injury (N = 28). We also excluded samples with SGs below 1.003 (N = 6) and above 1.050 (N = 6) as well as an additional five samples with very low creatinine levels (<0.05 ug/ul). We consequently retained 292 samples for analysis, averaging approximately nine samples per individual (range 3–20 samples).

Inferential Statistical Analyses

We performed Spearman’s rank correlations to assess bivariate relationships between dominance rank and aggression rates using the ‘corr.test’ function in R. Similarly, we performed a Spearman’s correlation to assess the relationship between average testosterone and creatinine levels. We used averages in all models to accommodate the mediation analyses (see below) and to maintain consistency across analyses. To generate testosterone and creatinine averages for each individual, we first derived residuals from linear models in which the predictors were variables understood to affect physiological parameters in wild chimpanzees. These variables included time of day of urine sample collection (Muller & Wrangham, 2004a), the presence of sexually receptive parous females with full sexual swellings (Muller & Wrangham, 2004b; Sobolewski et al., 2013) and the sine and cosine of Julian date, a method that captures nonlinear temporal variation in regression modelling (Stolwijk et al., 1999) and has been used to capture physiological seasonality in wild chimpanzees (Negrey et al., 2021; Wessling et al., 2018). To satisfy the assumptions of normality and homoscedasticity, we Box–Cox-transformed testosterone and creatinine prior to analysis (Box & Cox, 1964; Miller & Plessow, 2013). We then calculated the within-individual average of residuals for testosterone and creatinine, respectively, and weighted each individual in the model based on the number of urine samples collected for that individual, with greater weight given to individuals with more samples.

We then tested predictors of average testosterone and creatinine levels by constructing linear models (LMs) with Gaussian error structures using the ‘lm’ function in R. In the first LM, average testosterone level was the outcome variable and the predictors included dominance rank, total aggression rate and chimpanzee age (i.e. the average age at which urine samples were collected for a given individual), given that testosterone is expected to decrease with age (Muller, 2017). In the second LM, average creatinine level was the outcome variable. As with testosterone, the predictors were dominance rank, total aggression rate and chimpanzee age. We generated 95% profile likelihood confidence intervals using the ‘confint’ function.

To ease model convergence and produce comparable estimates for each predictor, we Z-transformed all predictors to a mean of 0 and a standard deviation of 1. We examined collinearity by checking variance inflation factors (VIFs), using the ‘vif’ function in the package ‘car’ (Fox et al., 2011). VIFs >5 are usually considered high. All VIFs in our models were <2.5. Model diagnostics (i.e. Shapiro–Wilk test, inspection of histograms and Q–Q plots) suggested the presence of an outlier with a very low creatinine level, so we ran the creatinine model again excluding this point. We consequently present results both including and excluding the outlier (see Results).

Given the results of multivariate regression, we further tested Hypothesis 2 (i.e. lean muscle mass links rank and testosterone) by performing causal mediation analyses using the function ‘mediate’ in the package ‘mediation’ (Tingley et al., 2014). Mediation was performed on modifications of the linear models described above, in which we used individual averages for testosterone and creatinine (i.e. one value per individual per variable). Each model included a given predictor, mediator and outcome as well as two control predictors: subject age (averaged across sample collection dates) and either creatinine (when testing Hypothesis 1) or aggression rate (when testing Hypothesis 2). Using the ‘MedPower’ app (Kenny, 2017), we calculated the expected statistical power for detecting each mediation effect using the beta coefficients derived from multivariate regression (Appendix, Table A1). As described previously, we identified one individual with very low creatinine levels as an outlier. We ran the mediation analysis with and without this individual, and we report the results of both analyses. We generated nonparametric bootstrap confidence intervals using the percentile method with 10 000 replicates. Alpha was set at 0.05 in all models.

RESULTS

Associations between Dominance, Aggression, Testosterone and Creatinine

Dominance rank was positively correlated with overall rates of aggression (Spearman rank correlation: rS = 0.55, P<0.001; Fig. 2). Urinary testosterone levels in adult male chimpanzees ranged from 0.01 to 3.1 pg/μl corr. SG (median ± SE: 0.62 ± 0.03). Results of a multivariate linear model in which testosterone was the outcome variable are presented in Table 1. Testosterone was positively associated with dominance rank (Fig. 3a) and negatively associated with overall aggression rate (Fig. 3b). Before correcting for SG, urinary creatinine values ranged from 0.05 to 2.6 μg/μl. Average creatinine residuals (derived from SG and its quadratic transformation) were significantly positively correlated with testosterone (Spearman rank correlation: rS = 0.40, P = 0.019; Fig. 3c). Results of multivariate linear models in which average creatinine residuals were the outcome variable, both including and excluding an outlier, are presented in Table 1. Creatinine residuals were positively associated with dominance rank with or without the outlier (Fig. 3d). Creatinine was not associated with aggression rates.

Figure 2.

Figure 2.

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Total aggression rate as a function of dominance rank in 34 adult male chimpanzees. Aggression rates were generated from 939 bouts of aggression and corrected for individual observation time (i.e. inclusion in scan samples). Dominance ranks were calculated from 582 male–male pant grunts using randomized Elo-ratings.

Table 1.

Results of linear models predicting average urinary testosterone and creatinine levels in 34 wild male chimpanzees

β SE 95% CI t P
Testosterone (R2adj = 0.28)
Intercept −0.002 0.144 [−0.295, 0.291]
Dominance rank 0.623 0.215 [0.183, 1.06] 2.89 0.007
Aggression rate −0.437 0.194 [−0.833, −0.041] −2.26 0.032
Age −0.725 0.184 [−1.10, −0.349] −3.93 <0.001
Creatinine, outlier included (R2adj = 0.09)
Intercept 0.055 0.147 [−0.244, 0.355]
Dominance rank 0.459 0.220 [0.010, 0.908] 2.09 0.045
Aggression rate −0.093 0.198 [−0.498, 0.311] −0.472 0.640
Age −0.332 0.188 [−0.716, 0.053] −1.76 0.088
Creatinine, outlier excluded (R2adj = 0.17)
Intercept 0.100 0.133 [−0.172, 0.372]
Dominance rank 0.434 0.198 [0.028, 0.840] 2.19 0.037
Aggression rate 0.009 0.182 [−0.363, 0.382] 0.051 0.959
Age −0.336 0.170 [−0.683, 0.011] −1.98 0.057
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We analysed creatinine with and without an extreme outlier; the results of both models are presented. The 95% confidence intervals (CIs) were generated using the profile likelihood. Values in bold and italic fonts represent P values <0.05 and <0.10, respectively.

Figure 3.

Figure 3.

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Associations between (a) dominance rank and testosterone, (b) aggression rate and testosterone, (c) testosterone and creatinine and (d) dominance rank and creatinine in 34 adult male chimpanzees. Testosterone and creatinine values are averaged residuals derived from linear models controlling for chimpanzee age as well as time and date of sample collection. Testosterone values in (a) and (b) were also accordingly corrected for dominance rank or aggression rate. Point size reflects the number of urine samples collected per individual. Dotted lines indicate upper and lower bounds of the 95% confidence interval. One individual with low creatinine levels has been excluded from (c) and (d).

Mediation Analyses

Results of mediation analyses are presented in Table 2. We did not find support for Hypothesis 1. On the contrary, aggression rate negatively mediated the (positive) association between dominance rank and testosterone (Table 2, Fig. 4a). We did, however, find support for Hypothesis 2: creatinine significantly positively mediated rank’s association with testosterone (Table 2, Fig. 4b, c). Hypothesis 2 was supported whether the one outlier was included or excluded (Table 2, Fig. 4b, c).

Table 2.

Results of mediation analyses

Model β 95% CI P Expected power
Dominance; aggression; testosterone
Average mediation effect1 −0.309 [−0.791, −0.010] 0.039 0.323
Average direct effect2 0.471 [0.041, 1.00] 0.031 0.412
Total effect3 0.162 [−0.229, 0.510] 0.402 0.147
Proportion mediated4 −1.90 [−21.9, 22.5] 0.437
Dominance; creatinine; testosterone
Outlier included Average mediation effect 0.152 [0.009, 0.360] 0.037 0.478
Average direct effect 0.471 [0.033, 1.01] 0.033 0.876
Total effect 0.623 [0.182, 1.15] 0.004 0.992
Proportion mediated 0.244 [0.014, 0.830] 0.039
Outlier excluded Average mediation effect 0.175 [0.001, 0.410] 0.049 0.606
Average direct effect 0.446 [0.007, 0.970] 0.048 0.877
Total effect 0.621 [0.180, 1.140] 0.003 0.991
Proportion mediated 0.282 [0.001, 0.950] 0.050
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For each analysis, variables are listed in the following order: main predictor; mediator; outcome. Testosterone and creatinine values were individual averages correcting for time of day of sample collection and the sine and cosine of sample collection date. Each value was weighted by the number of urine samples used to generate averages. All mediation models included chimpanzee age and aggression rate as control predictors. Nonparametric bootstrap confidence intervals (CIs) were generated using the percentile method with 10 000 replicates. ‘Expected power’ refers to the expected statistical power for detecting a mediation effect based on beta coefficients derived from multivariate regression; power was calculated using the ‘MedPower’ app (Kenny, 2017). Values in bold and italic fonts indicate P values <0.05 and <0.10, respectively.

1

‘Average mediation effect’, or average indirect effect, indicates the proportion of the main predictor’s association with the outcome variable attributable to the mediator or its effect on the outcome variable attributable to the mediator.

2

‘Average direct effect’ indicates the extent to which the main predictor directly predicts the outcome variable (i.e. not through the mediator).

3

‘Total effect’ refers to the combined direct and mediated/indirect effects.

4

‘Proportion mediated’ indicates the proportion of the total effect attributable to the mediation effect.

Figure 4.

Figure 4.

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Results of three mediation analyses testing (a) Hypothesis 1, (b) Hypothesis 2 (outlier included) and (c) Hypothesis 2 (outlier excluded). The predictor, mediator and outcome variables are listed above each plot. For each analysis, effects are listed vertically from top to bottom as follows: mediation (indirect) effect, direct effect and total effect (indirect effect plus direct effect). Points and horizontal bars indicate effect sizes and 95% confidence intervals, respectively.

DISCUSSION

In the present study, we tested whether high-ranking male chimpanzees exhibit high testosterone levels because they are more aggressive (Hypothesis 1) or have greater lean muscle mass (Hypothesis 2) than low-ranking males. We did not find evidence in support of Hypothesis 1. Surprisingly, although dominance rank was positively correlated with overall aggression rates, we found a negative relationship between aggression rate and testosterone. Furthermore, mediation analyses indicated ‘inconsistent mediation’, which occurs when one relationship between a main predictor, mediator and outcome is directionally opposite of all others (MacKinnon et al., 2006). In other words, the positive relationship between dominance rank and testosterone may have been partly masked by the negative relationship between aggression and testosterone. This is striking because high-ranking males both engage in high levels of aggression and exhibit relatively high testosterone levels.

This negative relationship between testosterone and aggression may reflect the intragroup bias characteristic of chimpanzee societies. Despite the presence of dominance-striving competition, intragroup homosocial relationships are strong and enduring among male chimpanzees (Mitani, 2009b), and intragroup aggression is usually much less severe than intergroup aggression (Wilson et al., 2014). Reliance on homosocial relationships may greatly impact testosterone’s relationship with aggression. For instance, among a sample of human males who perceived themselves to be interdependent, higher basal testosterone levels were associated with lower aggression levels (Welker et al., 2017). The quality of male–male relationships may therefore regulate testosterone’s links with aggression and explain, in part, the negative association between average testosterone levels and intragroup aggression in our data set.

Our results do not disprove the claim that testosterone can stimulate aggression in primates. For example, the absence of gonadal androgens decreases aggression in some castrated primates, including Japanese macaques, Macaca fuscata (Takeshitaet al., 2017) and common marmosets, Callithrix jacchus (Dixson, 1993). Adult male chimpanzees have average plasma and urine testosterone levels many times greater than do females, which has been attributed to higher rates of aggression and greater muscle mass in males than in females (Behringer et al., 2014; Sonnweber et al., 2022). Furthermore, various studies indicate that male chimpanzee testosterone levels rise in competitive environments in which aggression rate or the threat of aggression are heightened. For instance, both testosterone level and aggression rate increase in the presence of preferred mating partners that are sexually receptive (Muller & Wrangham, 2004a; Sobolewski et al., 2013). This pattern was upheld in our data: in a linear mixed model controlling only for subject identity, testosterone was higher in the presence of preferred, sexually receptive mating partners (β = 0.173, SE = 0.066, P = 0.009). Similarly, testosterone secretion increases during border patrols and intergroup encounters (Sobolewski et al., 2012), which can result in lethal aggression against members of neighbouring communities (Watts et al., 2006; Wilson et al., 2014).

The results of prior studies are generally consistent with the hypothesis that testosterone reactivity, or responsiveness to acute competitive provocation, promotes aggression. There is consistent and compelling evidence that the intensity of testosterone reactivity predicts aggressiveness (reviewed in Carré & Olmstead, 2015). This relationship has been observed, for instance, in captive male marmosets (Ross et al., 2004) and wild female baboons (Beehner et al., 2005) and likely applies to chimpanzees, such that intraindividual variation in testosterone secretion may predict aggression more effectively than average interindividual differences. Meanwhile, some research in humans suggests that the outcomes of competitive interactions inform testosterone secretion, such that victory is associated with increased testosterone levels (e.g. in badminton players; Jiménez et al., 2012). There also remains the possibility that other hormones moderate testosterone’s behavioural effects, for instance, that elevated cortisol levels reduce or inhibit testosterone-induced aggression (the dual-hormone hypothesis; Dekkers et al., 2019). Research of wild chimpanzees that analyses short-term changes in aggression (e.g. aggression rate per observation day) and/or the outcomes of aggressive interactions (e.g. ‘win’ or ‘loss’) with carefully matched urine sampling will help test these hypotheses, although such a study design is difficult to implement in free-ranging, group-living apes who must be studied noninvasively. Regardless, our results suggest that aggression is not sufficient to explain interindividual associations between dominance rank and testosterone level.

In contrast to Hypothesis 1, we found support for Hypothesis 2: urinary creatinine residuals, a proxy for lean muscle mass, were positively associated with both testosterone level and dominance rank, and creatinine significantly mediated dominance rank’s association with testosterone. These results are consistent with prior work from Ngogo showing that high-ranking male chimpanzees at Ngogo exhibit high core body temperatures (Negrey et al., 2020), a measure strongly positively linked to muscle mass in vertebrates (McNab, 2019). However, this is the first study, to our knowledge, to provide quantifiable evidence that dominance rank predicts a noninvasive measure of lean muscle mass in male chimpanzees. Curiously, this finding conflicts with prior work from Gombe Stream National Park, Tanzania, which found a clear relationship between body mass and dominance rank in females but not in males (Pusey et al., 2005). This disparity in our results may reflect greater statistical power in the Ngogo analyses due to a larger number of adult males and the treatment of rank as a continuous rather than categorical variable (Lazic, 2008) and/or to differences in group social dynamics.

Notably, causal relationships between testosterone, lean muscle mass and dominance rank are plausibly multidirectional. Testosterone levels likely contribute to greater lean muscle mass (Griggs et al., 1989), thereby increasing competitive ability in intrasexual contests. However, as suggested by population level analyses of humans (Ellison et al., 2002; Trumble et al., 2012), individuals with greater lean muscle mass likely enjoy greater energy intake and improved general health, which supports testosterone secretion. Indeed, well-fed, relatively inactive captive chimpanzees exhibit higher urinary testosterone levels than do wild chimpanzees (Muller & Wrangham, 2005). High-ranking individuals plausibly enjoy improved physical condition via preferential access to resources (Houle & Wrangham, 2021), although current evidence linking rank and energy balance in the genus Pan is equivocal (Emery Thompson et al., 2009; Surbeck et al., 2015). There are likely dynamic, multidirectional processes implicated in our results, however, and we cannot make causal claims at present, in part because our data represent a relatively short period of the total chimpanzee life span. Future studies tracking long-term variation in dominance rank, testosterone and lean muscle mass in chimpanzees will help unravel these relationships over the life course.

We acknowledge several notable differences between our methods and those of prior studies that may account for any discrepancies in our results. First, in contrast to prior studies (Muller & Wrangham, 2004a; Sobolewski et al., 2013), we corrected for urine concentration using specific gravity rather than creatinine, which allowed us to analyse testosterone and creatinine independently. Second, in addition to hydrolysis (Muller & Wrangham, 2004a), we performed solvolysis prior to testosterone measurement (Hauser, Schulz, et al., 2008), which increases the correlation between urinary and blood testosterone levels (Hauser et al., 2011). Third, we measured testosterone using a validated liquid chromatography–mass spectrometry (LC-MS) method instead of enzyme-linked immunoassays. Finally, we used multivariate rather than bivariate analyses (as in, for instance, Muller & Wrangham, 2004a), allowing us to test multiple predictors (e.g. aggression rates, urinary creatinine levels) simultaneously while controlling for variables such as age and time of day of sample collection.

Importantly, our results reflect two stable dominance hierarchies in one chimpanzee community. Males of this species are widely known to compete for reproductive opportunities through frequent and relatively severe acts of physical aggression (Wrangham et al., 2006). Therefore, our results may not apply to species in which aggression rates or between-individual variation in competitive investment are low. Similarly, despite evidence of considerable seasonal changes in body mass and composition in both male and female primates (Bergstrom et al., 2017; Bernstein et al., 1989; Hamada et al., 1986; Schiml et al., 1996) including chimpanzees (Pusey et al., 2005), it is not yet clear whether our findings apply to species in which male–male competitiveness varies greatly by season. Finally, not all strategies by which adult males achieve high rank hinge on physical size or intimidation (Foster et al., 2009). In humans, testosterone likely promotes many status-enhancing behaviours (Eisenegger et al., 2011), some of which are highly cooperative or even prosocial (e.g. generosity in rewarding cooperators; Boksem et al., 2013). Similarly cooperative effects of testosterone have been observed in males of other species (Kelly et al., 2022). Given that testosterone has been linked to nonaggressive behaviour in male chimpanzees (e.g. vocalization frequencies; Fedurek et al., 2016), testosterone may plausibly contribute to any number of status-enhancing behaviours in this species. For instance, because strong social bonds are crucial for the acquisition and maintenance of high rank (Bray et al., 2021; Nishida, 1983; Watts, 2000) and predict reproductive success (Feldblum et al., 2021), testosterone may promote intragroup male–male bonding. Exploring such alternatives is imperative for better understanding male primate mating effort and testosterone’s causal links with social status.

Data Availability

Data and R code generated for this study are available on figshare (https://figshare.com/s/93dc786398b0185e3ab6).

Highlights.

  • We examined rank, testosterone, aggression and creatinine in male chimpanzees.

  • Urinary testosterone levels were positively associated with male dominance rank.

  • Urinary testosterone levels were negatively associated with aggression rates.

  • Urinary creatinine was positively associated with dominance rank and testosterone.

  • Urinary testosterone mediated dominance rank’s association with urinary creatinine.

Acknowledgments

We thank the Uganda Wildlife Authority and Uganda National Council for Science and Technology for permission to work in Kibale National Park. For field and lab assistance, we thank Chris Aliganyira, Samuel Angedakin, Natasha Bartolotta, Verena Behringer, Charles Birungi, Charles Businge, Jeremy Clift, Rebecca Davenport, Sarah Dunphy-Lelii, Melissa Emery Thompson, Janette Gleiche, Emily Gregg, Claudia Herf-Collet, Brian Kamugyisha, Christina Kompo, Natalie Laudicina, Godfrey Mbabazi, John Mitani, Roger Mundry, Róisín Murtagh, Lawrence Ndangizi, Rachna Reddy, Carolyn Rowney, Joshua Rukundo, Aaron Sandel, Vera Schmeling, James Tibisimwa, Alfred Tumusiime, Ambrose Twineomujuni and David Watts. We also thank Cheryl Knott, Rachna Reddy and Ben Trumble for helpful conversations and comments on the manuscript. This work was supported by the Boston University Graduate School of Arts and Sciences, Nacey Maggioncalda Foundation, National Geographic Society (9824-15), U.S. National Institutes of Health (5R01AG049395), U.S. National Science Foundation (BCS-1613393) and Wenner-Gren Foundation.

Appendix

Table A1.

Results of multivariate regression models used to perform mediation analyses and calculate expected statistical power for mediation effects

Model Predictors β SE t P
Dominance; aggression; testosterone
Dominance → aggression Intercept −0.001 0.135 −0.010 0.992
Dominance rank 0.760 0.166 4.579 0.000
Creatinine −0.079 0.167 −0.472 0.640
Age −0.474 0.160 −2.968 0.006
Dominance + aggression → testosterone Intercept −0.020 0.138 −0.148 0.883
Creatinine 0.331 0.171 1.930 0.063
Dominance rank 0.471 0.221 2.134 0.041
Aggression rate −0.406 0.186 −2.181 0.037
Age −0.616 0.186 −3.319 0.002
Dominance; creatinine; testosterone (outlier included)
Dominance → creatinine Intercept 0.055 0.147 0.378 0.708
Dominance rank 0.459 0.220 2.088 0.045
Aggression rate −0.093 0.198 −0.472 0.640
Age −0.332 0.188 −1.761 0.088
Dominance + creatinine → testosterone Intercept −0.020 0.138 −0.148 0.883
Creatinine 0.331 0.171 1.930 0.063
Dominance rank 0.471 0.221 2.134 0.041
Aggression rate −0.406 0.186 −2.181 0.037
Age −0.616 0.186 −3.319 0.002
Dominance; creatinine; testosterone (outlier excluded)
Dominance → creatinine Intercept 0.100 0.133 0.751 0.459
Dominance rank 0.434 0.198 2.187 0.037
Aggression rate 0.009 0.182 0.051 0.959
Age −0.336 0.170 −1.982 0.057
Dominance + creatinine → testosterone Intercept −0.039 0.141 −0.280 0.782
Creatinine 0.403 0.194 2.073 0.048
Dominance rank 0.446 0.224 1.991 0.056
Aggression rate −0.434 0.191 −2.278 0.031
Age −0.590 0.189 −3.117 0.004
Open in a new tab

For each hypothesis, we include the results of two models: one in which the main predictor variable predicts the mediator and a second in which the main predictor and mediator both predict the main outcome variable. Values in bold and italic fonts denote P < 0.05 and 0.10, respectively.

Footnotes

Declaration of Interest

None.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Data and R code generated for this study are available on figshare (https://figshare.com/s/93dc786398b0185e3ab6).

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