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Flanged (A) and unflanged (B) male orangutans from Gunung Palung National Park, Indonesia, illustrating dramatic differences in morphology. Photos by Tim Laman.
Source publication
Male orangutans (Pongo spp.) display an unusual characteristic for mammals in that some adult males advance quickly to full secondary sexual development while others can remain in an adolescent-like form for a decade or more past the age of sexual maturity. Remarkably little is understood about how and why differences in developmental timing occur....
Citations
... The final transition from the unflanged to the flanged male morph occurs within a few months and is accompanied by a peak in testosterone levels (captivity: Maggioncalda et al., 1999;wild: Marty et al., 2015; rehabilitation centers: Prasetyo, 2019). Flanging is irreversible and its immediate triggering mechanism remains unknown, but has been linked to social factors (Emery Thompson et al., 2012), most prominently unstable dominance relationships among flanged males (Utami Atmoko & van Hooff, 2004). Our knowledge of reproductive success of the two morphs is limited, as siring opportunities are not only rare because of long female inter-birth intervals of 6-9 years (van Noordwijk et al., 2018), but also scattered in space because of orangutans' semi-solitary lifestyle (van Schaik, 1999). ...
In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross-sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long-term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross-sectionally in relation to population, male morph (unflanged and flanged), and other socio-ecological factors. Both our longitudinal and cross-sectional results confirm and refine previous cross-sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade-off between avoiding male-male contest competition and gaining mating access to females, and thus follow a "best-of-a-bad-job" mating strategy.
... These findings suggest that more studies include measurements of adult males with delayed expression of secondary sex characteristics beyond the range for puberty to gain insight into the regulation of growth, pubertal development, and sexual dimorphism. Unfortunately, data for unflanged male body size are scarce, especially for fully adult males, since males all develop flanges by age 17 or 18 years in captivity (Emery Thompson et al. 2012;Pradhan et al. 2012), and measuring body size in wild populations is inherently challenging, as darting and capturing wild apes for research is generally considered to be unethical and not permissible (Brown et al. 2022). Thus, natural history collections of wild orangutans offer an important opportunity to measure features that correlate with body size variation and, in turn, re-evaluate patterns of sexual dimorphism in this Asian great ape. ...
Among extant great apes, orangutans are considered the most sexually dimorphic in body size. However, the expression of sexual dimorphism in orangutans is more complex than simply males being larger than females. At sexual maturity, some male orangutans develop cheek pads (flanges) while other males remain unflanged even after becoming reproductively capable. Sometimes flange development is delayed in otherwise sexually mature males for a few years. In other cases, flange development is delayed for many years or decades, with some males even spending their entire lifespan as unflanged adults. Thus, unflanged males of various chronological ages can be mistakenly identified as ‘subadults’. Unflanged adult males are typically described as “female-sized”, but this may simply reflect the fact that unflanged male body size has only ever been measured in peri-pubescent individuals. In this study, we measured the skeletons of 111 wild adult orangutans (Pongo spp.) including 20 unflanged males, 45 flanged males, and 46 females, resulting in the largest skeletal sample of unflanged males yet studied. We assessed long bone lengths (as a proxy for stature) for all 111 individuals and recorded weights-at-death, femoral head diameters, bi-iliac breadths, and long bone cross-sectional areas (as proxies for mass) for 27 of these individuals, including seven flanged males, three adults confirmed-unflanged males, and three young adult likely-unflanged males. ANOVA and Kruskal-Wallis tests with Tukey and Dunn post-hoc pairwise comparisons, respectively, showed that body sizes for young adult unflanged males are similar to those of the adult females in the sample (all p ≥ 0.09 except bi-iliac breadth), whereas body sizes for adult unflanged males ranged between those of adult flanged males and adult females for several measurements (all p < 0.001). Thus, sexually mature male orangutans exhibit body sizes that range from the female end of the spectrum to the flanged male end of the spectrum. These results exemplify that the term ‘sexual dimorphism’ fails to capture the full range of variation in adult orangutan body size. By including adult unflanged males in analyses of body size and other aspects of morphology, not as aberrations but as an expected part of orangutan variation, we may begin to shift the way that we think about features typically considered dichotomous according to biological sex.
... It is still unknown how body and flange size correlate (i.e., do larger males have larger flanges?). This has important implications for understanding orangutan bimaturism, as the relationship between flange growth and other skeletal and developmental changes is still subject to ongoing research (e.g.,Dunkel et al., 2013;Emery Thompson et al., 2012). ...
We constructed a parallel laser photogrammetry apparatus constructed from commercially available parts, and measured forearm lengths and flange widths of 16 wild Bornean orangutans. Our objectives were to validate our method and apparatus, discuss issues encountered, and construct preliminary growth curves. For adult males, we also compared flange width to forearm length as a way to investigate the relationship between body size and flange development. We used a camera cage around a DSLR camera, on top of which we attached two parallel green lasers. We estimated error with repeatability, accuracy, and interobserver reliability measures, and measured forearm lengths in three different ways to see which was most consistent. The longest forearm measure was the most repeatable (CV = 1.64%), and was similar to flange repeatability (3.50%). Accuracy measurements of a known object were high (error = 0.25%), and Interobserver discrepancy low (3.74%). Laser spacing increased with distance to the subject, but we corrected for this using calibration photos after each session. We transparently discuss the issues we encountered with the aim that this accessible method can help expand the use of laser photogrammetry. Preliminary measurements show that male flange widths and forearm length do not reliably increase in tandem, and that female growth plateaus at around the age at first birth (15 years old). We conclude with suggested improvements to the apparatus and method to ensure the lasers remain parallel.
... Although the proximate mechanisms of orangutan bimaturism remain poorly understood (Emery Thompson et al., 2012;Maggioncalda et al., 1999;Marty et al., 2015), progress has been made on the question of its adaptive significance. Bimaturism is thought to reflect the combination of rare opportunities for fertilization by nondominant males, due to high operational sex ratios and the high reproductive skew (linked to both male dominance and female preference for flanged males) (Pradhan et al., 2012). ...
Orangutan females live semi-solitarily, spending 50–80 percent of their time alone, with only their dependent offspring for company (van Schaik, 1999). They are philopatric (Arora et al., 2012; van Noordwijk et al., 2002) and establish their home ranges in an area that overlaps with their natal range as well as with those of other females, both maternal relatives and nonrelatives (Ashbury et al., 2020; Morrogh-Bernard, 2009). Males disperse from their natal range as they become independent of their mother around the age of ten to twelve years (Nietlisbach et al., 2012) and settle far away from their natal area. Adult males are not territorial, and their home ranges overlap with those of females, but are far larger (Singleton et al., 2009). Determining male ranging patterns is challenging because their ranging area far exceeds the size of all study areas covered by earth-bound researchers, and individual males may not be around for several months or even years (Dunkel et al., 2013; Spillmann et al., 2017; Utami Atmoko et al., 2009a). In sum, orangutans have a dispersed social and mating system with high female site fidelity and widely roaming males.
... Fully "flanged" males exhibit pronounced cheek flanges, enlarged throat pouches, ropy hair, and increased body mass, and display pronounced differences in behavior, such as in long-calling rates, activity budgets, and interactions with females Knott et al. 2010). While flanged males produce higher levels of testosterone than unflanged males (Kingsley 1982;Maggioncalda, Sapolsky, and Czekala 1999), particularly if they developed early (Emery Thompson, Zhou, and Knott 2012), unflanged males are physiologically capable of siring offspring (Utami et al. 2002;Goossens et al. 2006). Given relatively late ages of first reproduction among captive orangutans compared with other great apes, it is reasonable to assume that wild orangutan males reach reproductive maturity late relative to their wild counterparts. ...
The living hominids share a suite of life history features that distinguishes them from other primates, including larger body size, extended juvenile growth and development, and a long lifespan. While modern humans exhibit many distinctions from their great ape relatives, these species provide an important reference by which to infer the life history characteristics of our last common ancestor. Demographic analysis of the great apes reveals specifically how life histories changed during recent human evolution and can provide perspective on inter-and intra-specific variation in life history features. In this chapter, we provide the most detailed information available on demographic characteristics of great apes, comparisons with humans, and discussion of the proximate factors that influence life history variation across the clade. 2
... Stress has been suggested as one such mechanism. However, results pertaining to the role of cortisol have been conflicting (Knott & Thompson, 2012, August;Maggioncalda et al., 2002;Marty et al., 2015;Prasetyo, 2019;Thompson et al., 2012). Captive and wild studies can provide conflicting results because in captivity, zoo orangutans rarely remain developmentally arrested into adulthood (Pradhan et al., 2012). ...
... Thus, captive studies do not include adult unflanged males in developmental arrest (Pradhan et al., 2012). Instead, they have adolescents who exhibit flange development later than other males but still within the adolescent phase, referred to as "arrested adolescents" (Knott & Thompson, 2012, August;Maggioncalda et al., 2002;Thompson et al., 2012). Only wild studies of orangutan populations contain adult unflanged males in developmental arrest. ...
... Although this is a common pattern in primates, it is not always the case, such as in male rhesus monkeys and chimpanzees which show the opposite pattern or no pattern with dominant males having higher or equal cortisol (Abbott et al., 2003;Bercovitch & Clarke, 1995;Kirchhoff, 2010). Hypothesis 1 also follows from studies showing elevated androgens in flanged male orangutans compared with unflanged males (Kingsley, 1982;Marty et al., 2015;Thompson et al., 2012). It could therefore be expected that flanged males would also have lower cortisol, since testosterone has been shown to have a negative relationship with cortisol in human males (Cumming et al., 1983;Hackney et al., 2017). ...
Objectives:
We compared an early life stress indicator, linear enamel hypoplasia (LEH), in the canine teeth of two male orangutan (Pongo spp.) morphs. Flanged males have large bi-discoid cheek pads and a laryngeal throat pouch, and they exhibit either the same or higher levels of the stress hormone cortisol throughout development compared with unflanged males, which lack secondary sexual characteristics. Such "developmental arrest" is hypothesized to either reflect a response to experienced high stress (Hypothesis 1), or an adaptation to avoid elevated stress levels and/or having experienced lower stress levels (Hypothesis 2) during early life. As LEH defect depth has been shown to reflect the severity (i.e., intensity and/or duration) of early life stress events, we examined whether unflanged males have shallower LEH defects than flanged males.
Materials and methods:
Flanging status was assessed by measuring the faces of preserved skins. Canine height (N = 37) was measured in the same individuals to assess commonality between morphs. LEH defect depths were analyzed using a standardized confocal profilometry method (N = 34).
Results:
Flanged males have significantly deeper LEH defects than unflanged adult males. Canine projected crown heights are similar across males regardless of morph.
Conclusions:
Evidence from great apes shows that, when comparing canines with similar growth patterns, deeper defects reflect more severe stress events during development. Thus, our results suggest that "developmental arrest" of unflanged males is not a response to having experienced stress, but rather an adaptation to avoid the physiological impacts associated with chronic stress and/or experiencing lower stress levels.
... This assay is commonly used for androgen quantification in various species, and with various biological matrices (polyclonal antiserum R156/7, provided by CJ Munro, UC-Davis)(Edwards et al., 2015;Emery Thompson et al., 2012;Herrick et al., 2010;Jacobs et al., 2014;Jaeggi et al., 2015;Narayan et al., 2013). Biochemical validation revealed parallelism between the binding inhibition curves of fecal extract dilution (range, 1:80-1:10,240) and testosterone standard (difference between slopes in the 20%-80% binding range: t = 0.392, p = .708), ...
Androgens are important mediators of male-male competition in many primate species. Male gorillas' morphology is consistent with a reproductive strategy that relies heavily on androgen-dependent traits (e.g., extreme size and muscle mass). Despite possessing characteristics typical of species with an exclusively single-male group structure, multimale groups with strong dominance hierarchies are common in mountain gorillas. Theory predicts that androgens should mediate their dominance hierarchies, and potentially vary with the type of group males live in. We validated the use of a testosterone enzyme immunoassay (T-EIA R156/7, CJ Munro, UC-Davis) for use with mountain gorilla fecal material by (1) examining individual-level androgen responses to competitive events, and (2) isolating assay-specific hormone metabolites via high-performance liquid chromatography. Males had large (2.6- and 6.5-fold), temporary increases in fecal androgen metabolite (FAM) after competitive events, and most captured metabolites were testosterone or 5α-dihydrotestosterone-like androgens. We then examined the relationship between males' dominance ranks, group type, and FAM concentrations. Males in single-male groups had higher FAM concentrations than males in multimale groups, and a small pool of samples from solitary males suggested they may have lower FAM than group-living peers. However, data from two different time periods (n = 1610 samples) indicated there was no clear relationship between rank and FAM concentrations, confirming results from the larger of two prior studies that measured urinary androgens. These findings highlight the need for additional research to clarify the surprising lack of a dominance hierarchy/androgen relationship in mountain gorillas.
... Dominant orangutan males display bimaturism in the form of extended growth of fatty cheek pads, which can develop at varying times in a male's lifetime, possibly dependent on the male's social environment (Kuze et al. 2005). Unflanged males housed in captivity with flanged males commonly experience delayed development of this secondary sexual trait, maintaining low testosterone levels and a phenotype similar to that of an adolescent male or female for years into adulthood (Kingsley 1982;Maggioncalda et al. 1999;Thompson et al. 2012). Flanged males are highly intolerant of each other, producing loud 'long calls' to delineate their territory and displacing and terminating consortships between unflanged males and females (Atmoko et al. 2009). ...
Objective
Sexual selection theory provides a framework through which some facial displays of male non-human primates can be investigated and understood. Here, we explore how both intra- and inter-sexual selection may influence facial morphology, physiology, and the behavior of male primates inhabiting diverse social and ecological environments.Methods
First, we will review how elements of the ecological environment, such as the spatio-temporal distribution of food, interacting with the diet of different species, shapes the social and mating systems of primates. In turn, these dynamics then influence how facial expressions, colors, and shapes are utilized in both the competition for and attraction of mates. We will focus on sexually dimorphic facial features that exhibit variation in their expression among males and that can be linked to differences in proxies of reproductive success.ResultsFacial displays can generally be divided into four types, each commonly associated with certain mating systems, social systems, and sexually selective pressures. Facial expressions, skin color, pelage, and variation in facial shape, can be involved in either mediating intra-sexual competition, mate choice, or a combination of both.Conclusions
Certain aspects of male non-human primate facial displays are likely to be shaped by processes of both intra- and inter-sexual selection. Accordingly, homologies and analogies between human and non-human primate facial displays can inform us of the processes of sexual selection that may have been operating throughout human evolution.
... Behaviorally, male mountain gorillas in Karisoke emigrate at 13.5 years and achieve dominance at 15 years on average (Robbins 1995). Male orangutans exhibit a rare phenomenon called bimaturism where individuals develop secondary sexual characteristics at variable time points or not at all (Emery Thompson, Zhou, and Knott 2012). Despite variability in the timing of flanging, all males likely attain sexual maturity around the same time (Maggioncalda, Sapolsky, and Czekala 1999). ...
... Testosterone may also play an important role in species where males' primary competitors are not their group mates. Male orangutans' transitions among various morphs (Maggioncalda 1995), from smaller, unflanged varieties lacking most or all adult secondary sex characteristics, to the largest flanged morph exhibiting full secondary sex characteristics, is associated with higher testosterone (Emery Thompson, Zhou, and Knott 2012;Marty et al. 2015). To our knowledge, no data on the relationship between competitive outcomes and testosterone have been published for western lowland gorillas, though in captivity, males housed with females, males housed in all-male groups, and males housed alone were found to have similar urinary androgen metabolite levels (Stoinski et al. 2002). ...
In many species androgens (e.g. testosterone) play an important role in male-male competition, mediating both intra- and inter-group competitive relationships. The connection between competition and androgens has been relatively well-studied in the genus Pan, but less so in other great apes. This chapter examines the relationship between urinary androgen metabolites (UAM) and dominance rank, as well as social group structure, in wild male mountain gorillas (Gorilla beringei). Data from two different time periods indicate there is no clear relationship between UAM and rank in this species. Instead, they suggest that any such connection might be mediated by the social dynamics among group members, including dominance hierarchy stability and/or the security of the dominant male’s tenure. There was also no clear relationship between UAM concentrations and social group structure. Males in multi- and single-male groups had similar concentrations, though very preliminary data suggest that solitary males might have lower UAM levels than their group-dwelling peers. Thus, there is weak support for the hypothesis that male mountain gorillas’ intrasexual competition is mediated by baseline androgen levels. They may therefore have more in common with bonobos (Pan paniscus) than chimpanzees (P. troglodytes) on this dimension, despite their extreme adaptations for male-male contest competition.
