Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx).код для вставкиСкачать
American Journal of Primatology 56:9–25 (2002) Developmental Variables and Dominance Rank in Adolescent Male Mandrills (Mandrillus sphinx) JOANNA M. SETCHELL1* AND ALAN F. DIXSON2 1 Subdepartment of Animal Behavior, University of Cambridge, Cambridge, United Kingdom 2 Center for the Reproduction of Endangered Species, Zoological Society of San Diego, San Diego, California Previous research on semifree-ranging mandrills has shown that the degree of secondary sexual development differs among adult males. While some males are social, brightly colored, and have large testes and high levels of plasma testosterone, other males are peripheral or solitary, and lack fully developed secondary sexual features. In order to determine how these differences among males arise, and to investigate the influence of social factors, we examined the adolescent development of 13 semifreeranging male mandrills of known age. Testicular volume began to increase markedly at 5.5 yr, and males began to develop secondary sexual adornments at the age of 6 yr. Males attained adult size and secondary sexual development at an average age of 9 yr. As males developed, they peripheralized, decreasing from 100% group-associated at 5 yr to 20% at 8 yr. At 9 yr some males reentered the social group and attained alpha rank, while others remained peripheral or solitary. Within this average development, there was marked variation among males in the timing of development. Adolescent males that were dominant for their age had higher testosterone levels, larger testes, and more advanced secondary sexual development than subordinate males. The implications of these findings are discussed in the light of differences that occur among adult males, male– male competition, and the evolution of secondary sexual adornments in this species. Am. J. Primatol. 56:9–25, 2002. © 2002 Wiley-Liss, Inc. Key words: secondary sexual development; sexual skin coloration; social rank; testicular volume; male–male competition INTRODUCTION Mandrills are extremely sexually dimorphic in body mass and secondary sexual traits [Darwin, 1871]. Adult males have a mean mass of 31 kg, 3.4 times that of females [Setchell et al., 2001]; brightly colored skin on the face, rump, and genitalia; bony supramaxillary swellings; long canines; a yellow beard; a long nuchal crest and cape; and an epigastric fringe of white hair [Hill, 1970]. Contract grant sponsor: Medical Research Council (UK). J.M. Setchell is now at the School of Life Sciences, University of Surrey Roehampton, London, UK. *Correspondence to: Dr. Joanna M. Setchell, School of Life Sciences, University of Surrey Roehampton, West Hill, London SW15 3SN, UK. E-mail: email@example.com Received 20 February 2001; revision accepted 16 October 2001 © 2001 Wiley-Liss, Inc. DOI 10.1002/ajp.1060 10 / Setchell and Dixson Unusually for an Old World monkey, mandrills have a sternal scent gland, which is larger and more active in males [Hill, 1970]. Great variation occurs among adult male mandrills in the degree of development of secondary sexual traits [Wickings & Dixson, 1992], and we have proposed that some male mandrills have suppressed secondary sexual development as part of an alternative reproductive strategy [Setchell & Dixson, 2001a]. High-ranking males have high levels of testosterone and invest in showy, metabolically expensive adornments which expose them to intermale competition and risk of injury. Such males mate-guard fertile females, while subordinate adult males have reduced investment in secondary sexual adornments, range on the periphery of the social group, and mate opportunistically. This may represent a tactic for economizing investment and ameliorating intermale competition [Setchell & Dixson, 2001a]. These differences among adult male mandrills raise the question of when during development an individual male’s strategy is determined. Primates are characterized by an extended period of adolescent development, between the juvenile and adult stages [Tanner, 1962]. This transition involves a suite of physical and social changes, culminating in reproductive and social maturity. Changes in males include somatic and skeletal growth, testicular development and maturation, and the ensuing development of secondary sex characters resulting from increased production of the gonadal steroid hormones. Few detailed studies exist of the timing and sequence of secondary sexual development in primates, with the exception of humans [e.g., Tanner, 1962; Malina, 1978]. The process of social development and changes in sexual and social behavior is better understood. For example, male dispersal is associated with reproductive maturation in almost all Cercopithecine species [Pusey & Packer, 1987]. An important question concerns the possible influence of the social environment on the timing and degree of adolescent development. In adolescent male rhesus macaques, agonistic rank correlates positively with testicular volume and testosterone levels at the onset of the mating season [Bercovitch, 1993], and in baboons higher-ranking adolescent males have larger testes for their age than lower-ranking males [Alberts & Altmann, 1995]. Maternal rank has also been shown to affect adolescent development in male rhesus macaques [Dixson & Nevison, 1997]. In order to investigate in detail how individual differences among adult male mandrills arise, and the factors that might influence such variation, we studied development from juvenile to adult status for known-age male mandrills living as members of a semifree-ranging colony. The aims of this report are twofold: first, to document patterns of growth in mass, crown-rump length, testicular volume, plasma testosterone levels, and the acquisition of secondary sexual adornments in male mandrills; and second, to investigate interrelationships between developmental variables, behavioral development in terms of emigration, and social factors such as dominance rank and maternal rank. METHODS Subjects Two groups of mandrills (n = 48 and n = 31), living in two naturally rainforested enclosures (6.5 ha and 3.5 ha, respectively), were studied at the International Medical Research Center in Gabon. Details of the history and management of the mandrill colony have been described by Setchell and Dixson [2001a,b]. We studied the behavior and development of 13 males (aged 5–9 yr) present in the two enclosures in March 1996 (Table I), over a period of 21 mo (March 1996–November 1997). We define “adolescence” as “that period of life beginning Adolescent Development in Male Mandrills / 11 TABLE I. Ages and Ranks of the Male Mandrills in Enclosures 1 and 2 ID Enclosure 1 Enclosure 2 2E 18b 12E 12A1 5C 2C1 5E 2G 2F 12C1 9b 16B 13b 14b 15b 12F 17C 10D Contributing ages (yrs) Rank within group Rank for agea Maternal ranka 8.0–9.7 — 7.9–9.7 9.0–10.8 9.1–10.8 6.9–8.6 7.0–8.7 6.0–7.8 6.6–8.4 5.1–6.8 — 8.0–9.7 — — — 6.9–8.7 6.1–7.8 6.9–8.7 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 High — High Low Low High Low High Low Low — High — — — Low High Low High — M Mid High High High High High Mid — Low — — — Mid Mid Mid a See Methods section. Table includes adult males, of estimated age, present in the enclosures during the study, that did not contribute data. b with the first visible signs of impending sexual maturity and ending with the cessation of linear growth and the attainment of adult size” [Watts, 1985]. Morphological Measurements Made at the Enclosures Sexual skin coloration measurements were made every 2 wk at a distance of 4 m while the animals were feeding. The brightness of the red/pink coloration on the nose, perianal field, dorsal margin of the rump, and penile shaft; blue sexual skin on the paranasal swelings and perineum; and violet coloration on the scrotum and just lateral to the ischial callosities were quantified using graduated color charts (published by the Royal Horticultural Society, London). The areas of skin affected by these colors was assessed using a five-point scale, where 0 = color as in an adult female, and 4 = maximum area affected [for details see Setchell, 1999; Setchell & Dixson, 2001b]. “Fattedness” of the rump was measured using rear-view photographs of males, taken from ground level at the feeding area, at a distance of 2–4 m. At least one good photograph was obtained per month for each male. Image analysis was used to calculate the area of the rump (cm2) from the photographs, using the width and height of the ischial callosities (measured for each male during captures) as a scale. Morphological Measurements Made on Anesthetized Males Males were captured and anesthetized on four occasions (March 1996, November 1996, April 1997, and October 1997) to collect morphological and endocrine data. Anesthesia was accomplished using a Telinject (Telinject USA, Inc., Saugus, CA) blowpipe to deliver a syringe containing Imalgene1000 (10 mg/kg; Rhone-Mérieux, Lyon, France). 12 / Setchell and Dixson The following measurements were made on each male: body mass (nearest 100 g), crown-rump length (nearest 5 mm), upper canine height (gingival margin to tip, nearest 1 mm), length (L) and width (W) of each testis (using calipers, and stretching the scrotal sac to exclude the epididymis from measurement), and length of cape hair, beard, and epigastric fringe (nearest 5 mm). Testicular volume was calculated using the formula for a regular ellipsoid: π 1/6.W2.L, and the volumes of the left and right testes were summed. Sternal glanduar development was rated using a five-point scale, where 0 = hairs the same as on the rest of the chest and abdomen, with no glandular secretion; 1 = hairs longer and thicker than surrounding hair but dry, with no glandular secretion; 2 = hairs longer, thicker, darker than surrounding hair, and slightly damp with secretion; 3 = hairs longer, thicker, darker than surrounding hair, and damp with secretion; and 4 = hairs longer, thicker, darker than surrounding hair, and wet with secretion. In addition to data collected during the study, information was available from the colony records, collected during annual veterinary health controls. This included measurements of mass (170 values from 38 males), canine height (103 values from 20 males), and testicular volume (104 values from 18 males). Blood Sampling and Testosterone Radioimmunoassay Blood (2.0 ml) was collected from the femoral vessels of anesthetized subjects during captures. Blood was centrifuged and plasma stored at –20°C until assayed for testosterone. All samples were collected between 1000–1200 hr in an attempt to minimize possible effects of diurnal changes in hormone levels, and 100-µl samples were assayed in duplicate for testosterone, using procedures previously described [Corker & Davidson, 1978; Setchell & Dixson, 2001c]. The assay detects testosterone at concentrations greater than 100 pg/ml. All samples were assayed at the same time, and intra-assay variation was 7.9%. Group Association and Dominance Rank Behavioral observations were made daily, between 0900–1200 and 1400–1700 hr, from a tower overlooking the enclosures. It was possible to observe the majority of animals on any given day, for variable periods of time, and a total of 602 hr (Enclosure 1) and 275 hr (Enclosure 2) of clear observation of social interactions were obtained. Ad libitum observations of approach–avoid and agonistic interactions were used to construct dominance hierarchies [Martin & Bateson, 1994]. In order to compare males of different ages, living in different groups, we determined whether each male was high-ranking or low-ranking for his age by plotting position in dominance hierarchy against age and examining the position of each male with respect to a regression line. Males that fell above the regression line were classified as subordinate for their age, and those below the line dominant for their age (Table I). Each male was scored daily as being “group associated”: traveling, feeding, and interacting as part of the social group; “peripheral”: often more than 100 m from other group members, traveling and feeding on the edge of the group; or “solitary”: traveling and feeding alone [after Wickings & Dixson, 1992]. Maternal Rank Female rank has been determined, using agonistic behavior and approach– avoidance interactions, since the inception of the colony, and shows few changes Adolescent Development in Male Mandrills / 13 over the years, other than those due to maturation or death [Setchell, 1999]. Maternal rank at the birth of a male was expressed as the percentage of females aged 3+ yr dominated [after Cheney et al., 1989], to account for demographic changes over time, and any changes in status. Maternal rank was then categorized into high (upper quartile), low (lower quartile), and middle (mid quartile range). Unfortunately, the sample included only one son of a low-ranking female. Investigations of the influence of maternal rank upon male development were therefore limited to the comparison of sons of high-ranking females (n = 6) with those of mid- and low-ranking females (n = 7). Statistical Analyses The 2-yr period of the study was not long enough to follow the development of individual males from juvenile (approximately 5 yr) to adult. In order to describe the average development of male mandrills for each characteristic of interest, we plotted all available data against age. Each male contributed 7–14 data points for mass, 4–6 points for crown-rump length, 4–6 points for testosterone, 4–11 points for testicular volume, 4–9 points for canine height, 4 points for sternal gland activity, 10–13 points for rump area, 22 points for each measure of sex skin color, and 22 points for group association. Data were treated as a mixed longitudinal and cross-sectional sample, and nonparametric locally-weighted leastsquares regression (lowess, f = 0.3) was used to fit curves to the data [Leigh, 1992; Moses et al., 1992]. Inspection of these average development curves allowed us to identify the “average” age at which developmental milestones were attained, and to determine “adult” values for characteristics, based on the maximum value for the average curve. The nature of the sample meant that we did not have “start” and “finish” ages for each male for each attribute. In order to compare the development of individual males with the average development curve for each trait, we calculated residuals from the lowess curve, as the natural logarithm of the ratio of the observed value to the expected value [Moses et al., 1992]. To avoid pseudoreplication of data, the residuals for each male for each trait were averaged to produce his development-for-age for that characteristic. The range of values of these mean residuals for individual males (“residual range”) was used to describe the extent to which males varied with respect to the average development curve. If individual males were consistently advanced or retarded in development, residuals for different traits would be positively correlated. To avoid performing multiple correlations on the same matrix of 13 males and 16 traits, we used principal-components analysis to explore interrelationships among traits. t-Tests were used to compare development-for-age scores for dominant vs. subordinate males, and to compare sons of high-ranking females with those of mid- and low-ranking females. RESULTS Overall Patterns of Development Incremental growth in body mass gradually declined from birth until the age of 2.5 yr, when mass velocity increased until reaching a peak at 7–8 yr. Males attained an adult mass of 31 kg by the age of 10 yr, although they gained very little mass after the age of 9 yr (mass 29 kg, 94% of adult mass (Fig. 1A)). Individual variation around the average development curve was large, and mass-forage residuals for individual males had a range of 0.32 in this sample. 14 / Setchell and Dixson Fig. 1. Development vs. age in male mandrills: (A) body mass, (B) crown-rump length, (C) plasma testosterone levels, (D) testicular volume, (E) upper canine height, (F) red coloration on the face, (G) rump area, and (H) percentage of days spent in the center of the social group. Points are individual measures of males. Lowess fitted curves (f = 0.3) show development of an “average” male. Crown-rump length growth rate declined from birth, with no marked adolescent growth spurt, and males reached an adult length of 72 cm at the age of 10 yr (Fig. 1B). As with mass, males aged 9 yr had very little length to gain (70 cm, 98% of adult crown-rump length). Crown-rump length-for-age was less variable than mass-for-age (residual range 0.13). Plasma testosterone levels were low (below 5 ng/ml) until the age of 7 yr (Fig. 1C), by which age males were at the peak of their growth spurt and the testes were 15 cm3 in volume. After 7 yr, testosterone levels were highly variable (range: 0.22–44.25 ng/ml), and it was impossible to determine an “adult” level of testosterone. The residual range for testosterone-for-age was very large (2.67). The testes descended at an average of 3.8 yr (±0.3, n = 15). They then remained small (combined volume < 4 cm3) until the age of 5.5 yr (Fig. 1D), when males weighed 12 kg, and were growing rapidly in mass. Testicular volume then increased linearly with age, reaching an average “adult” combined volume of 36 cm3 at 9 yr. Interindividual variation around the average development curve was large at all ages (residual range: 0.98), and testicular volume varied more than 10-fold in males aged 5–6 yr and 6–7 yr. The tips of the maxillary canines (2-mm points) first appeared at an average age of 4.75 yr, and an average adult canine height of 44 mm was attained at an Adolescent Development in Male Mandrills / 15 Fig. 1. (Continued) average age of 8.75 yr. Interindividual variation in canine development was very large (residual range: 3.04). The canines could emerge as late as 6.75 yr, and the earliest male to reach adult canine size did so a year earlier than average, at 7.75 yr (Fig. 1E). Red sexual skin coloration began to brighten on the muzzle, rump (red and pink), and genitalia (red and lilac) at 6 yr, shortly after the testes began to increase in size, but before testosterone levels began to increase markedly. Skin coloration took approximately 3 yr to fully develop, with average “adult” coloration achieved at 9 yr. The five measures of brightness followed very similar patterns, and color development is illustrated using red on the muzzle (Fig. 1F). Variation around average development was great for genital lilac (residual range 0.52), rump pink (0.56) and facial red (0.48), but less so for red around the tail (0.15) and on the genitalia (0.12). As pink and red brightened on the rump and genitalia, the area of skin affected by the color increased, and extent-for-age correlated positively with brightness-for-age in these areas (n = 13, rump pink r = 0.488, P = 0.091; genital red r = 0.622, P = 0.023). In contrast, red on the face did not spread beyond the nasal stripe (score 0) onto the eyes, brow, ears, and lips until 8.25 yr (range: 6.75–8.75 yr), when the red was already near maximal brightness, and facial red extent did not correlate significantly with red brightness (r = 0.211, P = 0.489). This score was extremely variable in older subadult males and young adults, and males 16 / Setchell and Dixson aged 8.5 yr could score from 0 (red on mid-stripe only) to 4 (maximum; brow, eyelids, ears, and lips bright red). In contrast to red sex skin color on the muzzle, the brightness and extent of the blue coloration on the paranasal ridges did not change as males developed. However, the blue on the rump, which occurred in a defined area below the ischial callosities, did increase in brightness with age. In young animals this blue coloration was pale. It began to brighten at an average age of 5.50 yr (range 5.00–6.75 yr), but did not change in extent. Adult blue coloration was almost luminescent, and was attained at 8.75 yr (range 7.25–8.75 yr). Developmental variation among individuals was moderate for blue brightness (residual range: 0.15). The first signs of chest gland secretory activity (score 2) occurred in males aged over 6.75 yr. Up to this age young males had noticeably different hair in the region of the sternal gland, but the gland itself was dry (score 1). An average adult sternal gland activity of 3 (hairs long, thick, dark, and damp with secretion) was attained at 9 yr. Variation in development was high (residual range 1.46). Males could score 3 as early as 7.25 yr, but could also have a dry sternal area (score 1) at all ages. The youngest male to show maximum secretion (score 4: hairs long, thick, dark, and wet with glandular secretion) was aged 8.75 yr. At 6 yr, young males had an epigastric fringe and beard measuring 5 cm, and a cape of 8 cm, very similar to mean adult female pelage (fringe 4 cm, beard 5 cm, cape 8.5 cm). Male pelage grew steadily longer from that age, reaching an average adult fringe length of 11 cm (range: 10–12 cm) at 9 yr, a beard of 8 cm (range: 8–9 cm), and a cape of 14 cm (range: 14–16 cm) at 10 yr. Variation around the average development curve was lower for beard length (residual range: 0.14) than for crest (0.36) or fringe development (0.47). Increase in male rump size with age is illustrated in Fig. 1G. A great deal of variation occurred around the average development curve (residual range: 0.52), and males appeared to follow two distinct trajectories of rump development. This difference between males was evident from the first age measured (6.4 yr), and became more extreme at 8 yr, when larger-rumped males increased more quickly in “fattedness,” while smaller-rumped males did not. After 9.5 yr, when individual males showed little further increase in rump “fattedness,” large-rumped males (n = 4, mean ± SEM = 763 ± 9 cm2) had 30% larger rumps than smallrumped males (n = 5, 566 ± 12 cm2, t7 = 12.72, P < 0.001). Males up to age 5 yr were permanently associated with their social group. As testes increased in size, testosterone levels increased, and secondary sexual characteristics began to develop, males began to spend time on the edge of their group (Fig. 1H). By age 7 yr, males spent, on average, 50% of days peripheral to the group or completely solitary. This process of emigration was, however, enormously variable among individuals. At the extremes, one male aged 7 yr was still 100% group-associated, while another 7-yr-old was always peripheral or solitary. At 8.5 yr, some males began to reassociate with their group, resulting in an upward trend in the average group-association curve, although other males remained solitary. The final downward trend in the curve can be attributed to the two oldest contributing males being solitary. Interrelationships Among Developmental Variables Principal-components analysis of 16 trait-for-age residuals for the 13 males identified two factors that explained a total of 53.8% (factor 1, 31.7%; factor 2, 22.1%) of the variance in development (illustrated in Fig. 2). All 16 developmental variables examined loaded positively on axis 1, indicating a general trend for Adolescent Development in Male Mandrills / 17 Fig. 2. Factor loading plot resulting from principle-components analysis of 16 developmental variables-forage for 13 adolescent male mandrills. male mandrills to be early or late in developing. Thus, if a male was well developed for one characteristic, he was also well developed for other traits. Body size (mass and crown-rump length), testosterone concentration, testicular volume, blue and red sex skin color, and sternal gland activity loaded highly on this “general maturity factor 1.” Within this pattern, testicular volume and testosterone fell very close together, meaning that males with high testosterone for their age also had large testes for their age. The two measures of body size—crown-rump length and mass—were also close together, indicating that males that were heavy for their age were also long for their age. Measures of sex skin color and sternal gland activity also formed a cluster along axis 1, close to mass and crown-rump length. Thus, males that were large for their age also exhibited well-developed coloration and had active sternal glands for their age. Measures of pelage length, fattedness, and canine height were more independent of “general maturity factor 1,” loading less positively on this axis. The three measures of pelage (beard, cape, and epigastric fringe) were clustered together, but separated from other traits, meaning that (corrected for age) although a male with a long beard would also have a long cape and fringe, he was not necessarily well developed for other traits. Fattedness of the rump was quite separate from body mass, indicating that fattedness was a separate phenomenon, and that males with large rumps were not simply heavier than those with small rumps. 18 / Setchell and Dixson Influence of Male Dominance and Maternal Rank The dominance rank of males, calculated from avoidance reactions and submission, is included in Table I. As expected, rank was closely associated with age, with older adolescent males outranking younger males in general (age vs. rank: group 1: rs = –0.817, n = 9, P = 0.007). However, in group 2, where only four adolescent males were present, no significant correlation occurred (rs = –0.800, n = 4, P = 0.200). Males that were dominant for their age scored significantly higher for the general maturity factor than did males that were subordinate for their age (dominant males score (n = 7) 0.588 ± 0.281, subordinate males (n = 6) –0.824 ± 0.305, t = 3.35, P = 0.007). Specifically, dominant males were more mature than subordinates as regards testicular volume, plasma testosterone, blue and red sex skin color, and sternal gland activity (Table II). Up to the age of 8.5 yr, dominant males were significantly less group-associated than subordinate males (group association for age residual for dominant males (n = 4) –1.01 ± 0.20, subordinate males (n = 4) –0.03 ± 0.24, t6 = 3.13, P = 0.020). Beyond the age of 8.5 yr, the most dominant, brightly colored males (n = 3) began to reenter their social groups, while subordinate males of this age (n = 2) remained solitary or peripheral (sample sizes are too small for statistical comparison). The relationship between dominance rank and actual measurements of males is illustrated in Fig. 3, which shows average (lowess) development curves for dominant and subordinate males for selected characteristics. Dominant males had consistently brighter coloration, up to 20% larger testes, very much higher testosterone, and became less than 50% group-associated 9 mo earlier than did subordinates. The effect of dominance rank on mass was transient and small, with a maximum of 3 kg difference (dominants 13% heavier than subordinates) at 7–8 yr. Maternal rank had a small influence on male mass, with sons of high-ranking mothers being heavier for their age than sons of mid- or low-ranking mothers (P = 0.052 (Table III)). This effect is illustrated in Fig. 4. Sons of high-ranking mothers had an average advantage of 1 kg (age 2–7 yr) or 2 kg (7+ yr) over sons of low-ranking mothers. However, maternal rank was not significantly associated with the male’s “general maturity factor 1” score (sons of high-ranking mothers (n = 6) 0.268 ± 0.470, sons of mid-/low-ranking mothers (n = 7) –0.268 TABLE II. Effect of Dominance Rank on Adolescent Development in Male Mandrills Mean (SEM) development for agea Developmental variable Body mass Crown-rump length Testicular volume Plasma testosterone Red color Blue color Sternal gland activity Rump “fattedness” Beard length Cape length Epigastric fringe length Canine height a High ranking (N = 7) –0.001 (0.030) 0.016 (0.010) 0.072 (0.080) 0.789 (0.319) 0.024 (0.010) 0.063 (0.025) 0.111 (0.190) –0.020 (0.074) 0.012 (0.012) 0.026 (0.056) –0.012 (0.029) –0.211 (0.182) Low ranking (N = 6) t11 P –0.052 (0.041) –0.004 (0.019) –0.203 (0.107) –0.176 (0.180) –0.030 (0.013) –0.097 (0.052) –0.440 (0.126) –0.007 (0.071) –0.001 (0.022) –0.020 (0.022) –0.067 (0.053) 0.125 (0.349) –1.04 –1.00 –2.10 –2.51 –3.29 –2.92 –2.33 0.12 –0.54 –0.70 –0.95 0.89 0.322 0.337 0.060 0.029 0.007 0.014 0.040 0.904 0.599 0.497 0.364 0.392 Data are development for age residuals (see Methods section for further explanation). Adolescent Development in Male Mandrills / 19 Fig. 3. Development vs. age for dominant and subordinate male mandrills: (A) body mass, (B) plasma testosterone levels, (C) testicular volume, (D) red coloration on the face, and (E) percentage of days spent in the center of the social group. Points are individual measures of males. Lowess fitted curves (f = 0.3) show development of an “average” male. 20 / Setchell and Dixson TABLE III. Effect of Maternal Dominance Rank on Adolescent Development in Male Mandrills Mean (SEM) development for agea Developmental variable High ranking mother (N = 6) Body mass Crown-rump length Testicular volume Plasma testosterone Red color Blue color Sternal gland activity Rump “fattedness” Beard length Cape length Epigastric fringe length Canine height 0.026 (0.034) 0.019 (0.020) 0.008 (0.100) 0.262 (0.319) 0.003 (0.046) 0.011 (0.014) –0.028 (0.182) –0.031 (0.071) 0.007 (0.015) –0.014 (0.034) –0.030 (0.059) –0.371 (0.207) a Mid-/Low-ranking mother (N = 7) t11 P –0.068 (0.027) –0.004 (0.008) –0.110 (0.110) 0.413 (0.350) –0.023 (0.054) –0.012 (0.017) –0.242 (0.209) 0.002 (0.078) 0.005 (0.018) 0.021 (0.053) –0.043 (0.023) 0.213 (0.269) 2.18 1.17 0.78 –0.32 0.36 1.05 0.76 –0.31 0.11 –0.54 0.23 –1.68 0.052 0.267 0.450 0.758 0.723 0.318 0.464 0.763 0.911 0.597 0.823 0.122 Data are development for age residuals (see Methods section for further explanation). ± 0.342, t11 = 0.92, NS), nor with any other aspect of development except mass (Table III). Dominant males were not necessarily sons of high-ranking females: the median maternal rank of dominant males was 60% of females dominated, vs. 75% for subordinate males (Mann-Whitney U = 20, Z = –0.14, NS). Nor did ma- Fig. 4. Mass for age for sons of high-ranking (black circles, unbroken line) and mid- or low-ranking (open circles, dashed line) mothers. Points are individual measures of males. Lowess fitted curves (f = 0.3) show development of an “average” male. Adolescent Development in Male Mandrills / 21 ternal rank significantly influence the age at which males emigrated (group association-for-age residual: high-ranking mother, n = 6, –0.344 ± 0.370, mid-/lowranking mother, n = 7, –0.689 ± 0.319, t6 = 0.71, NS). DISCUSSION The sequence of events that occurs as male mandrills develop from juvenile to adult status is summarized in Fig. 5. Testicular volume begins to increase at an average of 5.5 yr, an event which is linked with the production of mature sperm in primates [Dang & Meussy-Dessolle, 1984]. The age at onset of puberty in male mandrills is thus similar to that reported for other Cercopithecine species [Bercovitch, 2000], and for female mandrills, which conceive for the first time at an average age of 4.25 yr [Setchell et al., in press]. However, at this stage males are only 39% of adult mass, and resemble females in appearance. At 6 yr, males begin to develop secondary sexual characteristics, and by 9 yr they have attained adult testicular volume, striking sex skin coloration, an active sternal gland, long upper canines, a beard, cape, and epigastric fringe, and have very little more mass to gain. Males thus attain reproductive maturity almost 5 yr after females first reproduce, and incur the substantial metabolic costs of increasing in mass (becoming 3.4 times the mass of females), and developing secondary sexual characteristics. Fig. 5. Sequence and timing of events during adolescent development in male mandrills. Bars represent the average age at which a trait begins to develop and reaches adult levels (from lowess curve fitting). The range of ages below the start and finish of each bar indicates the extent of variation among males. Group association: age at emigration = age at which males start to spend <50% days in the center of the group; age at reimmigration = age at which males start to spend >50% days in the center of the group. Blanks occur where some males do not achieve the threshold. Testosterone levels are too variable to determine the age at which “adult” levels are attained. 22 / Setchell and Dixson As they increase in size and develop sex skin coloration and an active sternal gland, male mandrills also peripheralize from their social group. They are only rarely group-associated at the height of the growth spurt. This solitary phase may represent a tactic to minimize potential social factors constraining growth and development while maximizing increases in body size prior to immigration into a new group, as in long-tailed macaques (Macaca fascicularis [van Noordwijk & van Schaik, 1985]). In this captive situation males rejoin their natal group. It seems likely that in the wild they might disperse and join other groups, but this remains unknown. Marked individual variation occurs in development, with a general trend to be early or late in developing, as in rhesus macaques [Watts, 1985], and human beings [Tanner, 1978; Bielicki et al., 1984]. A mass threshold that is necessary, but not sufficient, for reproductive maturation has been proposed for female primates [Frisch & McArthur, 1974; Frisch, 1984], and the positive relationships among mass, testicular volume, testosterone, and secondary sexual development suggest that the same may be true for male mandrills. The delays in development of the secondary sexual characteristics, which occur in some male mandrills, have also been noted in proboscis monkeys, uakaris, and orang-utans [Fontaine, 1981; Kingsley, 1982, 1988; Bennett & Sebastian, 1988; Graham & Nadler, 1990], and, in orang-utans at least, they appear to be related to dominance rank. Like subordinate male mandrills, “arrested” adolescent orang-utan males have lower concentrations of androgens (testosterone and dihydrotestosterone) than developing males [Maggioncalda et al., 1999]. Arrested males also have lower concentrations of luteinizing hormone and urinary growth hormone [Maggioncalda et al., 2000], implicating both the hypothalmic-pituitarytesticular axis and other neuroendocrine pathways. Similar effects of dominance rank upon male reproductive maturation have been demonstrated for rhesus macaques [Bercovitch, 1993] and baboons [Alberts & Altmann, 1995], where higher-ranking adolescent males have larger testes for their age than lower-ranking males. Reduced secondary sexual development in subordinate male mandrills is likely to be a consequence of lower testosterone levels in these males. Red sex skin color is known to be androgen-related [Vandenburgh, 1965; Rhodes et al., 1998; Setchell & Dixson, 2001a]. Blue scrotal coloration is rank-dependent in vervets [Brain, 1965; Gartlan & Brain, 1968; Isbell, 1995], although it is not androgen-dependent in adult male talapoins [Dixson & Herbert, 1974], patas monkeys [Bercovitch, 1996], or mandrills [Setchell & Dixson, 2001a]. Are differences among males a result or the cause of dominant or subordinate status in adolescent male mandrills? Prepubertal differences in body mass are likely to affect the dominance rank of age-mates, with heavier males dominating lighter age-mates [Lee & Johnson, 1992; Pereira, 1995]. Studies manipulating captive groups of primates show that high levels of testosterone are a result rather than a predictor of high dominance rank [Sapolsky, 1993]. Thus, heavier male mandrills are dominant, therefore have higher testosterone levels, and hence develop secondary sexual traits faster and to a greater extent than lighter males. Low testosterone levels in subordinate males may be due to stressinduced suppression of testicular function [Sapolsky, 1985; Graham & Nadler, 1990]. Differences in the hormone responsiveness of tissues may also be important. In rhesus macaques, testosterone acts as a pro-hormone in the control of sex skin coloration and is converted to estrogen in the target organ [Rhodes et al., 1998]. There may be fewer enzymes available for the conversion of testosterone to estradiol (aromatase) or DHT (5-α-reductase), or the receptor population Adolescent Development in Male Mandrills / 23 for hormones may differ in subordinate males. Feeding competition, and/or metabolic efficiency may also play a part in reducing the development of subordinate males [Bercovitch, 2000]. Finally, sons of high-ranking female mandrills had a mass advantage over sons of lower-ranking mothers. One might therefore expect that these slight differences in mass would affect a male’s rank, and the maternal rank would therefore influence the secondary sexual development of sons, with sons of high-ranking mothers being dominant and developing faster than sons of low-ranking mothers. It is possible that the lack of a significant influence of maternal rank on son’s rank, secondary sexual development, or emigration in this study was due to the lack of sons of very low-ranking females, and the small sample size. As in male baboons [Alberts & Altmann, 1995], opportunity is likely to be the most important influence upon dominance rank in male mandrills, and in small samples this may obscure any effect of maternal rank on male development. In conclusion, this report has documented for the first time the patterns of growth and the striking secondary sexual changes that occur in male mandrills as they pass through puberty and attain adulthood. Marked individual differences in the timing of testicular function, sexual skin coloration, and other features are also apparent in males, as well as differences in the ages at which they emigrate from their natal groups. These differences correlate most strongly with male dominance rank, so that high-ranking males develop faster and emigrate earlier than subordinate males in mandrill social groups. ACKNOWLEDGMENTS We are grateful to the Centre International de Recherches Médicales, Franceville (CIRMF) for permission to study the mandrill colony, and for providing accommodations to J.M.S. during the study. We thank Jean Wickings and the past and present staff of the Primate Center for keeping records of the mandrills over the past 17 years; Hamish Fraser and Fiona Pitt of the MRC Reproductive Biology Unit, Edinburgh, for help with testosterone assays; and Phyllis Lee for helpful discussion. J.M.S. was supported during data collection by a Medical Research Council (U.K.) Ph.D. studentship. REFERENCES Alberts S, Altmann J. 1995. Preparation and activation—determinants of age at reproductive maturity in male baboons. Behav Ecol Sociobiol 36:397–406. Bennett EL, Sebastian AC. 1988. Social organisation and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak. Int J Primatol 9:233– 255. Bercovitch FB. 1993. Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil 99:113–120. Bercovitch FB. 1996. Testicular function and scrotal coloration in patas monkeys. J Zool Lond 107:93–100. Bercovitch FB. 2000. Behavioral ecology and socioendocrinology of reproductive maturation in cercopithecine monkeys. In: Whitehead PF, Jolly CJ, editors. Old World monkeys. Cambridge: Cambridge University Press. p 298–320. Bielicki T, Koniarek J, Malina RM. 1984. Interrelationships among certain measures of growth and maturation rate in boys during adolescence. Ann Hum Biol 11:201. Brain CK. 1965. Observations on the behavior of vervet monkeys (Cercopithecus aethiops). Zool Afr 1:13–27. Cheney DL, Seyfarth RM, Andelman SJ, Lee PC. 1989. Reproductive success in vervet monkeys. In: Clutton-Brock T, editor. Reproductive success. Chicago: University of Chicago Press. p 384–402. Corker CS, Davidson DW. 1978. A radioimmunoassay for testosterone in various biological fluids without chromatography. J Steroid Biochem 9:373–374. Dang DC, Meussy-Dessolle N. 1984. Quan- 24 / Setchell and Dixson titative study of testis histology and plasma androgens at onset of spermatogenesis in the prepubertal laboratory-born macaque (Macaca fascicularis). Arch Androl 12:43–51. Darwin C. 1871. The descent of man and selection in relation to sex. London: John Murray. 475 p. Dixson AF, Herbert J. 1974. The effects of testosterone on the sexual skin and genitalia of the male talapoin monkey. J Reprod Fert 38:217–219. Dixson AF, Nevison C. 1997. The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta). Horm Behav 31:126–135. Fontaine R. 1981. The uakaris, genus Cacajao. In: Coimbra-Filho A, Mittermeier RA, editors. Ecology and behaviour of neotropical primates. Rio de Janeiro: Academia Brasiliera de Ciencias. p 443– 493. Frisch RE, McArthur J. 1974. Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185:949–951. Frisch RE. 1984. Body fat, puberty, and fertility. Biol Rev 59:161–188. Gartlan JS, Brain CK. 1968. Ecology and social variability in Cercopithecus aethiops and C. mitis. In: Jay P, editor. Primates: studies in adaptation and variability. New York: Holt, Rhinehart Winston. p 102–145. Graham C, Nadler R. 1990. Socioendocrine interactions in great ape reproduction. In: Zeigler TE, Bercovitch FB, editors. Socioendocrinology of primate reproduction. New York: Wiley Liss. p 33–58. Hill WCO. 1970. Primates, comparative anatomy and taxonomy. Vol. VIII. Cynopithecinae, Papio, Mandrillus, Theropithecus. Edinburgh: Edinburgh University Press. 680 p. Isbell LA. 1995. Seasonal and social correlates of changes in hair, skin, and scrotal condition in Vervet monkeys (Cercopithecus aethiops) of Amboseli National Park, Kenya. Am J Primatol 36:61–70. Kingsley S. 1982. Causes of non-breeding and the development of the secondary sexual characteristics in the male orang-utan: a hormonal study. In: de Boer L, editor. The orang-utan: its biology and conservation. The Hague: Dr. W. Junk Publishers. p 215–229. Kingsley S. 1988. Physiological development of male orang-utans and gorillas. In: Schwartz J, editor. Orang-utan biology. New York: Oxford University Press. p 123–131. Lee PC, Johnson J. 1992. Sex differences in the acquisition of dominance status among primates. In: Harcourt A, de Waal F, editors. Cooperation and competition in animals and humans. Oxford: Oxford University Press. p 391–414. Leigh S. 1992. Patterns of variation in the ontogeny of primate body size dimorphism. J Hum Evol 23:27–50. Maggioncalda AN, Sapolsky RM, Czekala NM. 1999. Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. Am J Phys Anthropol 109:19–32. Maggioncalda AN, Czekala NM, Sapolsky RM. 2000. Growth hormone and thyroid stimulating hormone concentrations in captive male organgutans: implications for understanding developmental arrest. Am J Primatol 50:67–76. Malina RM. 1978. Adolescent growth and maturation: selected aspects of current research. Yearb Phys Anthropol 21:63–94. Martin P, Bateson PPG. 1994. Measuring behaviour: an introductory guide. 2nd ed. Cambridge: Cambridge University Press. 222 p. Moses L, Gale L, Altmann J. 1992. Methods for analysis of unbalanced, longitudinal growth data. Am J Primatol 28:49–59. Pereira M. 1995. Development and social dominance among group living primates. Am J Primatol 37:143–175. Pusey AE, Packer C. 1987. Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 250–266. Rhodes L, Argersinger ME, Gantert LT, Friscino BH, Hom G, Pikounis B, Hess DL, Rhodes WL. 1998. Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques. J Reprod Fert 111:51–57. Sapolsky RM. 1985. Stress-induced suppression of testicular function in the wild baboon—role of glucocorticoids. Endocrinology 116:2273–2278. Sapolsky RM. 1993. Endocrinology al fresco: psychoendocrine studies of wild baboons. Recent Prog Horm Res 48:437–453. Setchell JM. 1999. Socio-sexual development in the male mandrill (Mandrillus sphinx). PhD thesis. University of Cambridge. Setchell JM, Dixson AF. 2001a. Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx). Am J Phys Anthropol 115:245–252. Setchell JM, Dixson AF. 2001b. Circannual changes in secondary sexual characteristics, gonadal function and sexual behavior in semifree-ranging mandrills (Mandrillus sphinx). Am J Primatol 53:109–121. Setchell JM, Dixson AF. 2001c. Changes in Adolescent Development in Male Mandrills / 25 the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177–184. Setchell JM, Lee PC, Wickings EJ, Dixson AF. 2001. The ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). Am J Phys Anthropol 115:349–360. Setchell JM, Lee PC, Wickings EJ, Dixson AF. Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). Int J Primatol. In press. Tanner JM. 1962. Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity. 2nd ed. Oxford: Blackwell Scientific. 326 p.. Tanner JM. 1978. Fetus into man: physi- cal growth from conception to maturity. Cambridge, MA: Harvard University Press. 280 p. van Noordwijk M, van Schaik C. 1985. Male migration and rank acquisition in wild long-tailed macaques (Macaca fascicularis). Anim Behav 33:849–861. Vandenburgh JG. 1965. Hormonal basis of the sex skin in male rhesus monkeys. Gen Comp Endocrinol 5:31–34. Watts E. 1985. Adolescent growth and development of monkeys, apes and humans. In: Watts E, editor. Nonhuman primate models for human growth and development. New York: Liss. p 41–65. Wickings EJ, Dixson AF. 1992. Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx). Physiol Behav 52:909–916.