Are badges of status adaptive in large complex primate groups?

Abstract

Sexual dimorphism in ornamentation in primates may have been sexually selected as signals of rank and dominance to males or by augmenting attractiveness to females. While male primates display tremendous variation in secondary sexual traits, such as sexual skin, capes of hair, and beards, which are often attributed to sexual selection, their phylogenetic distribution remains to be fully understood. Here we investigate the hypothesis that sexual dimorphism in ornaments is more pronounced in larger more ‘anonymous’ social organizations where quick reliable assessment of male quality, social status, dominance, and aggressiveness are selective pressures. Multiple regression analyses, including phylogenetic correction, were performed on 154 species representing 45 genera of simian primates. We found a positive relationship between degree of ornamental dimorphism and group size, even after controlling for other independent variables such as habitat type (i.e. openness of terrain) and fission-fusion dynamics. Dimorphism was also significantly associated with social organization, so that males from species with multilevel social organizations had the highest ratings for ornamentation. In sum, our analysis suggests that among primates with larger group sizes and multilevel social organizations, males have more developed visually conspicuous secondary sexual traits. This may reflect selection for amplified signals of individual identity, rank, dominance, or attractiveness in large and complex social organizations wherein social and physical conflict may arise frequently and individual recognition is limited.

Full text

Original Article
Are badges of status adaptive in large complex primate groups?
Cyril C. Grueter
a,
⁎,KarinIsler
b
, Barnaby J. Dixson
c
a
School of Anatomy, Physiology and Human Biology, The University of Western Australia, Crawley/Perth WA 6009, Australia
b
Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland
c
Evolution & Ecology Research Centre, School of Biological, Earth & Environmental Sciences, University of New South Wales, Kensington, Sydney, Australia
abstractarticle info
Article history:
Initial receipt 15 July 2014
16 February 2015
Final revision received 6 March 2015
Available online xxxx
Keywords:
Ornaments
Sexual selection
Sexual dimorphism
Primates
Sexual dimorphism in ornamentation in primates may have been sexually selected as signals of rank and domi-
nance to males or by augmenting attractiveness to females. Whilemale primates display tremendous variationin
secondary sexual traits, such as sexual skin, capes of hair, and beards, which are often attributed to sexual selec-
tion, their phylogenetic distribution remains to be fully understood. Here we investigate the hypothesis that
sexual dimorphism in ornaments is more pronounced in larger more ‘anonymous’social organizations where
quick reliable assessment of male quality, social status, dominance, and aggressiveness are selective pressures.
Multiple regression analyses, including phylogenetic correction, were performed on 154 species representing
45 genera of simian primates. We found a positive relationship between degree of ornamental dimorphism
and group size, even after controlling for other independent variables such as habitat type (i.e. openness of ter-
rain) and fission–fusion dynamics. Dimorphism wasalso significantly associated with social organization,so that
males from species with multilevel social organizations had the highest ratings for ornamentation. In sum, our
analysis suggests that among primates with larger group sizes and multilevel social organizations, males have
more developed visually conspicuous secondary sexual traits. This may reflect selection for amplified signals of
individual identity, rank, dominance, or attractiveness in large and complex social organizations wherein social
and physical conflict may arise frequently and individual recognition is limited.
© 2015 Elsevier Inc. All rights reserved.
1. Introduction
Male primates express a diverse array of conspicuous colorful, hairy,
and fleshy traits. Their marked sexual dimorphism strongly suggests a
role of sexual selection in their origins, either as badges of status or at-
tractive ornaments (Andersson, 1994; Darwin, 1871). Examples include
the elongated noses in proboscis monkeys (Nasalis larvatus), cheek
flanges in orang-utans (Pongo spp.), capes of white and silvery-grey
hair in hamadryas baboons (Papio hamadryas), reddened chests in
geladas (Theropithecus gelada), upper-lip warts in golden snub-nosed
monkeys (Rhinopithecus roxellana), and beards in humans (Homo sapiens;
Dixson, Dixson, & Anderson, 2005).
At least some of these ornaments may enhance male sexual attrac-
tiveness to females (Dixson, 2012). Female Bornean orang-utans, for
example, mate more often with males with fully developed cheek-
flanges than un-flanged males around ovulation (Knott, Thompson,
Stumpf, & McIntyre, 2010). Red and blue coloration in the mandrill
(Mandrillus sphinx) may advertise genetic diversity around the MHC
(Setchell, Charpentier, Abbott, Wickings, & Knapp, 2010; Setchell &
Huchard, 2010). The red skin that covers the head and face in the red
uakari (Cacajao calvus) becomes paler during times of sickness, suggesting
that disease may affect the expression of male ornamentation (Nunn &
Altizer, 2006). Male rhesus macaques (Macaca mulatta)withdarkerred
facial coloration receive more sexual solicitations from a greater number
of females during the mating season than paler faced males (Dubuc,
Allen, Maestripieri, & Higham, 2014). However, many factors affect male
mating success and it remains to be demonstrated among other species
whether mating success is determined by the attractiveness of secondary
sexual ornaments and whether male ornaments associated with genetic
benefits enhance sexual attractiveness.
Pronounced sexual dimorphism in body mass and canine size has
been well documented in male primates (Plavcan, 2012) and is func-
tionally linked to the frequency and intensity of male competition
(Grueter & van Schaik, 2009; Plavcan & van Schaik, 1992, 1997). There
is mounting evidence that visually conspicuous adornments serve as
badges of status, signalling dominance rank within sexes (Dixson,
2012). Such ornaments function in concert with body size during
male–male agonistic interactions, where cues that signal strength and
fighting ability to conspecific competitors may serveto curtail the prob-
ability of conflicts escalating into fights (Barrette & Vandal, 1990;
Maynard-Smith, 1982). Mature male western gorillas (Gorilla gorilla)
have more muscle mass and are larger than females, with silvery gray
hair on their backs and a bony-adipose crest on top of the head. Males
with the largest adipose crests have the most females in their one-
male units (Caillaud, Levréro, Gatti, Ménard, & Raymond, 2008)and
crest size is significantly correlated with offspring survival and the
annual rate of siring offspring that survive to weaning age (Breuer,
Robbins, Boesch, & Robbins, 2012). The expression of fully developed
Evolution and Human Behavior xxx (2015) xxx–xxx
⁎Corresponding author. School of Anatomy, Physiology and Human Biology, The
University of Western Australia, Crawley/PerthWA 6009, Australia.Tel.: +61 8 6488 8643.
E-mail address: cyril.grueter@uwa.edu.au (C.C. Grueter).
http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003
1090-5138/© 2015 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
Evolution and Human Behavior
journal homepage: www.ehbonline.org
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

cheek flanges and beards in male orang-utans depends on gaining
dominant status (Galdikas, 1985; Kingsley, 1982; Utami Atmoko &
van Hooff, 2004). Red facial coloration in male mandrills is positively
associated with social dominance (Setchell & Dixson, 2001a; Wickings
& Dixson, 1992), with gain of higher social rank (Setchell & Dixson,
2001b), and reproductive success (Wickings & Dixson, 1992). Similarly,
male drills (Mandrillus leucophaeus) can be up to three times the size of
females, possess large canines, and marked sexual dimorphism in
coloration. Brightness of male ornaments correlates with greater domi-
nance rank and reproductive success (Marty, Higham, Gadsby, & Ross,
2009). The redness of the skin patch on the chest of male geladas is
also brighter among those males with larger harems, whereas bachelor
and secondary follower males have more muted coloration (Bergman,
Ho, & Beehner, 2009).
Primates live in diverse social organizations that differ markedly in
their sizes and composition. The strength of conspicuous ornaments in
conveying male rank, dominance, and social status may vary depending
on the composition and size of the social group. The functional value of
such ornaments is expected to be particularly high in large and fluid
groups in which social knowledge is limited (Bergman, 2010; Bergman
& Sheehan, 2013; Bergman et al., 2009; Marty et al., 2009; Setchell &
Kappeler, 2003). For example, male mandrills spend long periods of
time in isolation before joining large hordes of females after they have
entered tumescence (Abernethy, White, & Wickings, 2002). In such a
scenario where males do not develop long-term bonds between social
or breeding partners, the evolution of highly conspicuous signals of
male rank and dominance may facilitate rapid recognition of male dom-
inance, rank, and status involved in intra-sexual competition and possi-
bly female choice (Dixson, 2012). Among geladas and hamadryas
baboons, both of which live in multilevel polygynous societies wherein
one-male units are part of higher-level social groupings and in frequent
contact, sexual selection may have shaped the evolution of conspicuous
signals of rank and dominance (Bergman & Sheehan, 2013; Bergman
et al., 2009). Conversely, in smaller cohesive groups, individual recogni-
tion and more frequent interactions may allow animals to better assess
the social status, strength, and quality of their contemporaries and po-
tentially reduce the selective pressures for external ornaments
(Kappeler & van Schaik, 2004). Thus, among species that exist in larger
social groups, ornaments may be better developed than among smaller
groups. Indeed, recent comparative analyses reported a positive correla-
tion between group size and complexity of facial color patterns in Old
Word monkeys and apes (Catarrhini; Santana, Alfaro, Noonan, & Alfaro,
2013). The catarrhines differ from New World monkeys (Platyrrhini),
where color patterns have evolved to facilitate individual recognition in
small social groups (Santana et al., 2013). Further, Old Word monkeys
that are highly gregarious and sympatric express more complex facial
color patterns than species characterized by non-gregarious and non-
sympatric social organizations (Santana et al., 2013), as do New World
monkeys living in small social groups with high levels of sympatry
(Santana, Alfaro, & Alfaro, 2012).
The properties of the environment and therisk of predation may also
impact on theexpression of ornamentation between species. In guppies
(Poecilia reticulata), while male coloration is under strong sexual selec-
tion via female choice (Houde, 1997), polymorphisms in ornamental
color patterns between populations might reflect a compromise be-
tween conspicuously signalling attractiveness and crypsis (Endler,
2000). In agamid lizards, concealed sexually dichromatic ornaments
are better developed among species living in closed than open habitats
(Stuart–Fox & Ord, 2004). Primates also occupy variable habitats, from
open savannahs to densely forested areas and the intensity of coloration
may be inversely related to darkness of the environment (Chaplin &
Jablonski, 1998;seealsoMarchetti, 1993). Interestingly, catarrhines
that live in more densely forested and humid habitats have more darkly
pigmented faces (Santana et al., 2013). Kamilar and Bradley (2011) also
found a positive effect of evotranspiration on pelage darkness across
primates. Thus, in addition to social structure, ecological factors are
associated with diversity in the complexity of color patterning in facial
ornaments and pelage among primates.
Despite mounting evidence that among male primates secondary
sexual traits serve as ornaments that attract females and as badges of
status between males, their phylogenetic distribution remains to be
fully understood. In the present study we employ a quantitative mea-
sure of sexual dimorphism in ornamentation,including all hairy, fleshy,
and colorful adornments, in a cross-species comparative approach to as-
sess the evolution of ornamentation in male primates. We analyzed
phylogenetic regression models using data from simian primates
representing 154 species from 45 genera. We base our predictions on
the theory that male–male competition and female choice have shaped
the evolution of visually conspicuous sexually dimorphic traits in male
primates. Recent comparative evidence reveals that facial color pattern-
ing is more complex among catarrhines living in larger and more sym-
patric social groups (Santana et al., 2013; see also Allen, Stevens, &
Higham, 2014). Thus, we use group size as a proxy for the degree of ‘so-
cial anonymity’(Bergman et al., 2009; Moffett, 2013) and predicted that
the selective pressures for signalling status to male conspecifics and at-
tractiveness to females result in greater male ornamentation in species
with larger group sizes. There is also evidence that individuals in larger
groups spread out as a counterstrategy to scramble competition (e.g.
Snaith & Chapman, 2008), thus exacerbating the perceived level of
‘anonymity’. Further, the social composition of the group and the extent
to which species exhibit fission–fusion dynamics characterized by fre-
quent flux in group membership may put a premium on readily apparent
signals of rank, dominance, and attractiveness. The degree to which each
species exhibits group cohesion both over long and short timescales was
included in the model as a possible contributing factor influencing orna-
mentation. We also included habitat type as a potential factor predicting
ornamental diversity across species. Mating system has also been shown
to correlate with dimorphism in male visual traits, with polygynous spe-
cies scoring highest for sexual dimorphism in adornments (Dixson et al.,
2005). Here we extend this work to test how social aspects of sexual
selection might generate selective pressures for signals of rank and
attractiveness. Thus, we included a refined classification of primate social
organizations as a predictor variable and tested this against mating
systems in our analysis to test the prediction that species with multilevel
social organizations have higher scores for ornamentation.
2. Methods
2.1. Quantifying sexual dimorphism in ornaments
Sexual dimorphism in every discernible ornament was quantified
using a 6-point rating scale (Dixson et al., 2005), where 0 = no diffe-
rence between males and females (e.g., both sexes have a crest of hair
of the same size and color); 1 = a very slight difference with the visual
trait slightly more developed in males than in females; 2 = a small but
notable difference in males compared with females; 3 = moderate dif-
ference;4 = large difference between the sexes; 5= a very large differ-
ence (e.g. males possessing a prominent visual trait that is absent, or
virtually so, in females). Scores were then summed for a total ornamen-
tation value (range 0–32). All parts had the same weight in the final
score. Rating scales of this type have been validated in comparative
studies of primate genital morphology (Dixson, 1987; Harcourt & Gardiner,
1994; Verrell, 1992) and visually conspicuous ornaments (Santana et al.,
2012, 2013), facilitating statistical and phylogenetic comparisons across
a broad spectrum of genera and species.
In the presentstudy ratings for all sexually dimorphic visual traits in-
volving the trunk, limbs, and head for a total of 154 species representing
45 genera of New World monkeys, Old World monkeys and apes, in-
cluding humans were used. The majority of the data were taken from
Dixson et al. (2005) and the dataset was refined and extended to in-
clude a few additional species, particularly in the genera Rhinopithecus,
Semnopithecus,Trachypithecus and Cercopithecus. Scoring was done by
2C.C. Grueter et al. / Evolution and Human Behavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

visual inspection of photographs (n=4–12 per species; mixture of front,
side, back views, and faces) and drawings and descriptions in Rowe and
Myers (2011), Arkive (www.arkive.org), Mittermeier, Rylands, and
Wilson (2013) and the first author's personal photographic library. We
tried to minimize the potential confounding effect of varying light levels
by selecting a representative sample of photographs with different light
conditions. Most of the photos were professional and hence well ex-
posed. The effects of polymorphisms and intraspecific variation were re-
duced in our analyses by scoring all traits at their maximal expression
(e.g. fattened males in mandrills and flanged males in orang-utans)
and by garnering photos from as many different populations as possible.
Table 1 provides details of how the scoring system was applied to
quantify degrees of expression for each trait. Examples of traits that
are visually conspicuous but present in equal degrees in both sexes
(score = 0) include the bright pink lips of the black-and-white snub-
nosed monkey (Rhinopithecus bieti), beards in black colobus monkeys
(Colobus satanas), the moustache in both sexes of the emperor tamarin
(Saguinus imperator), and the very similar red sexual skin on the rump
and genitalia of the rhesus macaque (Macaca mulatta). Examples of in-
termediate scores of 1–3 include the beard of the male brown howler
monkey (Alouatta fusca/guariba), which is only slightly larger than the
female (score = 1). The hairless red skin on the scalp and face of adult
red uakaris is marginally accentuated in adult males compared to fe-
males due to the prominence of their temporal muscles (score = 2).
The scrotal tuft of the male Peruvian yellow-tailed woolly monkey
(Oreonax flavicauda) is also somewhat more pronounced in the male
than the female (score = 2). The cheek hair (whiskers) appear mode-
rately more pronounced in the male long-tailed macaque (Macaca
fascicularis) than the female (score = 3). In some cases intermediate
scores in the Likert scale were assigned. For example, in adult mandrills
both the male and female have pronounced yellow beards and nuchral
crests of hair. However, they appear more pronounced inthe male than
the female and were ascribed a score of 3.5 respectively as they judged
as falling between moderate to large in their sexual dimorphism (AF
Dixson personal communication). In contrast, the vivid red and blue
facial sexual skin and prominent boney paranasal ridges are highly
sexually dimorphic in the mandrill and both received a score of 5.
Other examples of pronounced dimorphism include the much larger
and pendulous nose of male proboscis monkeys compared to the
female's much smaller snub nose (score = 5). In the golden snub-
nosed monkey, adult males have bulbous flaps on the upper lip on
each side of the mouth, which are absent or vestigial in females
(score = 5). Similarly, the flanged male Bornean orang-utan has large
cheek flanges that are absent in females (score = 5). Finally, in adult
human males, we included the occurrence of facial hair (beard and
moustache: score = 5), male pattern baldness (in some individuals:
score = 2.5), and body hair (score =2.5). Examples of the degree of di-
morphisms in ornaments are provided in Table 1 and the full data set
with descriptions of the individual traits for each species are provided
in Table S1 (available on the journal's website at www.ehbonline.org).
Some secondary sexual traits undergo changes as a result of rank re-
versals (Setchell & Dixson, 2001a, 2001b). However, in our analysis we
considered signals at their maximum level of expression. The only spe-
cies that are characterized by sexual dichromatism in pelage color were
Nomascus concolor,Nomascus gabriellae,Nomascus leucogenys,Hylobates
pileatus,Hoolock/Bunopithecus hoolock,Pithecia pithecia,Alouatta caraya,
and Alouatta fusca. Sexually dichromatic traits (pelage dimorphism)
may be accounted for in terms of sexual selection, but this is far from re-
solved (Bradley & Mundy, 2008). Hence, we calculated two separate
scores of ornamental dimorphism for those species: one that included
both dimorphism in pelage color and ornaments and one that is based
on ornaments only.
2.2. Group size
Primates vary markedly in the sizes of their groups. Bornean orang-
utans, for example, are non-gregarious (van Schaik & van Hooff, 1996)
whereas mandrills move in hordes of up to 600–800 individuals
(Abernethy et al., 2002; see also Grueter & Zinner, 2004 for other exam-
ples of primates living in extremely large groups). To investigate the effect
of social group size on ornamentation, we used a measure of group size
defined as the number of individuals typically in a social group. For spe-
cies living in multilevel organizations with more than one distinct level
of social organization we used band size (Grueter, Chapais, & Zinner,
2012). For species with fission–fusion dynamics we used community
size (Aureli et al., 2008). Group size data were collated primarily from
Rowe and Myers (2011) and Campbell, Fuentes, MacKinnon, Bearder,
and Stumpf (2011), supplemented with data from Grueter (2009, 2013;
if not otherwise noted in Table S2, available on the journal's Web site at
www.ehbonline.org). Group sizes were calculated using species means
and if ranges were given we took the midpoint. For humans we used a
group size of 490, which is the average community size of a representa-
tive sample of hunter–gatherer across the globe (Layton & O'Hara, 2009).
2.3. Habitat type
A habitat type was considered open if the species occurred in savan-
nah, open woodlands (e.g. ‘savannah baboon’), alpine grasslands (e.g.
geladas), limestone formations (‘limestone langurs’). Dense forests
were considered closed habitats. Habitat data were obtained from
Table 1
Examples of how the Likert-type scale was applied to scoring visually conspicuous secondary sexual traits in monkeys, apes, and humans.
012 3 45
Hairy traits (e.g. capes, tufts, and beards)
Saguinus imperator—the
moustache is equally
developed in both
sexes
Semnopithecus
achates—male facial
hair slightly longer
than in the female
Pithecia monachus—male has some
buffy hairs on the crown of the head
Macaca fascicularis—male has more
prominent cheek hair (‘whiskers’)
than female
Pongo
pygmaeus—male's
beard is much larger
than female's
Homo sapiens—male
beard is markedly
more prominent than
in females
Fleshy traits
Rhinopithecus bieti—the
bright pink lips are
equally developed in
both sexes
Rhinopithecus
avunculus—slightly
longer corkscrew
hair on male tail than
the female
Cacajao calvus—both sexes lose hair
and have reddened facial skin that is
accentuated in the male due to their
larger temporal muscles
Papio hamadryas—male has red sex
skin on rump, which resemble that
of the female but differs in
morphology from the female's
swelling
Pongo pygmaeus—male
has a fatty/fibrous
hump on top of head
that is very sexual
dimorphic
Pongo
pygmaeus—male has
markedly larger cheek
flanges
Colourful traits
Macaca mulatta—the red
sexual skin on the
rump and genitalia is
very similar between
the sexes
Rhinopithecus
brelichi—red hair on
back of their head
Cacajao calvus—the male's bulging
temporal muscles and other features
make his red head appear visually
more striking than that of the female
Cercopithecus diana—Blue scrotum. Rhinopithecus
bieti—pelage is much
more contrastingly
colored in males
Pithecia pithecia—male
has a white face mask
and black pelage that
are lacking in females
3C.C. Grueter et al. / Evolution and HumanBehavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

Rowe and Myers (2011) and Campbell et al. (2011;seeTableS2,
available on the journal's Web site at www.ehbonline.org).
2.4. Fission–fusion
We also recorded whether a given species exhibits fission–fusion,
defined as fluctuating patterns in group cohesion both over long- and
short timescales (Grueter, Chapais, et al., 2012). Species with male in-
fluxes during breeding such as patas monkeys (Erythocebus patas)
were also scored as fission–fusion. We note that fission–fusion dynamics
vary within-species. For example, muriqui (Brachyteles arachnoides)
form stable social groups but also fission–fusion. Further, detailed infor-
mation is missing for many species. In our analyses we used the model
category of fission–fusion for each species compiled from Mittermeier
et al. (2013),Campbell et al. (2011),andGrueter, Chapais, et al. (2012),
but we acknowledge that these data are somewhat coarse-grained (see
Table S2, available on the journal's Web site at www.ehbonline.org).
2.5. Social organization and mating system
Previous work has shown that mating systems, whichcategorize the
principle systems in which sexual behavior and reproduction occur, in-
fluences ornamental dimorphism in primates (Dixson et al., 2005). In
the present study we extended this research to test how social compo-
nents of sexual selection might also generate selective pressures for the
need to signal rank, dominance, and attractiveness. Thus, in addition to
mating system, we tested how social group organizations predict varia-
tion in male ornamentation. We distinguished among the following
types of social organization: multimale–multifemale (n=56species),
singlemale–multifemale (n= 39), singlemale–singlefemale (28),
multimale–singlefemale (7), and multilevel (10). Multilevel societies
encompass two or morenested grouping levels and represent “social ar-
rangements in which regular or constant proximity as well as coordi-
nated activity among [socio-spatially distinct] subunits [typically one-
male units] is the norm”(Grueter, Matsuda, Zhang, & Zinner, 2012;
pp. 993–994). Semi-solitary orang-utans did not fall into any of these
categories, and were therefore unclassified. There is also variation
within-species in social organization. For example, mountain gorillas
(Gorilla beringei beringei) live in single male and multi-male groups
(Stoinski et al., 2009). In the present study we used the modal social
organization for each species using data compiled from Willems,
Hellriegel, and van Schaik (2013) and complemented with data from
Mittermeier et al. (2013) and Grueter (2009).
2.6. Body mass and body mass dimorphism
Previous work has shown that scores for sexually dimorphic visual
traits in male primates are positively correlated with the degree of sexual
dimorphism in body mass (Dixson et al., 2005). Thus, we included
female body mass and body mass dimorphism, respectively, as control
variables in the phylogenetic models. Data on body mass and body
mass dimorphism (Table S2, available on the journal's website at
www.ehbonline.org) were obtained from Smith and Jungers (1997),
Isler et al. (2008) and Mittermeier et al. (2013).
2.7. Data analyses
Because of the interspecific nature of the dataset, we fitted phyloge-
netic regression models using phylogenetic generalized least squares
(PGLS), to control for phylogenetic non-independence. The phylogeny
of primates including branch lengths was based on Perelman et al.
(2011). Some species were excluded from analyses, as they were not
in the tree: Mico nigriceps,Pygathrix cinerea,Saguinus inustus,
Trachypithecus delacouri. A few species were replaced by closely related
species in the tree: Cercopithecus sclateri by Cercopithecus erythrotis,
Oreonax flavicauda by Lagothrix cana,andSemnopithecus ajax by
Semnopithecus dussumieri.
We constructed four models: (1) a model in which group size was
regressed against dimorphism in visual traits; (2) a model containing
group size plus social organization, fission–fusion dynamics, habitat
type, and female body mass as control predictor variables and their
two-way interactions with group size. Since none of the interactions
were significant, we did not retain them in the final models; (3) a
model containing the same variables as in model #2 with the exception
of female body mass, which was replaced by sexual dimorphism in body
mass; (4) a model containing the same variables as in model #2 with
the exception of social organization, which was replaced by mating sys-
tem; including both mating system and social organization in the same
model yielded a singularity, as the two variables are exactly collinear.
For species with sexual dichromatism, entering a composite score
including both dimorphism and dichromatism did not alter the output
in the single-predictor and multi-predictor models, so for phylogenetic
regression we disregarded the contribution of dichromatism on dimor-
phism in visual traits.
We undertook natural log data transformations to conform with as-
sumptions of parametric statistical models (we added ‘1’to each value
of zero in the table, as the natural log of zero is not defined). Phylogenetic
generalized least-squares (PGLS) analyses were conducted using the
caper package (Orme, Freckleton, Thomas, Petzoldt, & Fritz, 2011)inthe
R 2.15 computing environment (R Develpopment Core Team, 2012).
The parameter lambda was estimated jointly within the regression con-
text using a maximum likelihood procedure (Nunn, 2011). All analyses
were two-tailed and we consider p≤0.05 to be statistically significant.
3. Results
3.1. The relationship between group sizes and male ornaments
Phylogenetic linear regressions revealed a statistically significant
effect of group size on sexual dimorphism in ornamentation among
simian primates (model#1; F=32.1;R
2
=0.178;pb0.0001; DF =1,
148; n=150;λ=0.967;Table 2). There was a significant positive re-
lationship between group size and male ornamentation so that males
from species with larger groupsizes scored significantlyhigher for orna-
mentation than species with smaller group sizes (Fig. 1). Mandrills re-
ceived the highest score of 32 for adornments and had one of the
largest group sizes of 481. Drills also received a high score of 24.5 and a
social group size of 58. Geladas and hamadryas baboons both received
adornment scores of 13 and had group sizes of 156.2 and 85.6 respectively.
The gray snub-nosed monkey (Rhinopithecus brelichi) also received a high
score of 12 and lives in large social groups of up to 400. Species in which
the scores for ornamentation were low and the group sizes were smaller
included Cercopithecus, Saguinus and Trachypithecus (Tables S1 and S2,
available on the journal's Web site at www.ehbonline.org).
3.2. The effect of group size, social organization, mating system, fission–
fusion dynamics, habitat type, female body mass, and body mass dimorphism
on ornamentation
We then tested the effect of group size on ornamentation in a model
that included social organization fission–fusion dynamics, habitat type,
and female body mass (model #2). The overall model fit was statistically
Table 2
Parameter estimatesfor phylogenetic regression of group size (xvariable) and visual trait
dimorphism (y variable).
Predictor Estimate Std error tp
Intercept -0.167 0.716 -0.23 0.8169
Ln group size 0.380 0.067 5.67 b0.0001
4C.C. Grueter et al. / Evolution and Human Behavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

significant (F=10.36;R
2
= 0.391; pb0.0001; DF =9,129;n=138;
λ= 0.955). Among the individual predictors in the model, neither habi-
tat type, fission–fusion, or female body mass explained a significant
amount of variation. However, group size and social organization both
had a highly significant influence on visual trait dimorphism (Table 3).
Thus, species living in larger groups with multilevel social organizations
exhibited the highest levels of dimorphism in visual traits (Fig. 2).
Geladas and hamadryas baboons represent the species characterized
by multilevel social organizations with the highest scores for ornamen-
tation, both receiving 13. The four species of snub-nosed monkeys
(Rhinopithecus), each of whom have multilevel social organizations,
also received generally high scores for ornamentation ranging from 5
among Tonkin snub-nosed monkeys (Rhinopithecus avunculus)to12
among gray snub-nosed monkeys (Table S1, available on the journal's
Web site at www.ehbonline.org). Higher scores for visual trait dimor-
phism in these multilevel species are consistent with the prediction
that multilevel social organizations lead to elaboration of expression
of ornamental features.
Model #3, which contained body mass dimorphism instead of fe-
male body mass, produced a significantly positive effect of body mass
dimorphism, but did not change the significant effects of group size
and social organization found in model #2 (F= 12.41; R
2
= 0.435;
pb0.0001; DF = 9, 129; n= 138; λ= 0.955) (Table S3, available on
the journal's Web site at www.ehbonline.org).
Replacing social organization with mating system led to a weaker
model (model #4), with mating system not exerting an effect on orna-
mentation and the positive association between group size and orna-
mentation remaining (F= 10.1; R
2
=0.352;pb0.0001; DF =8,130;
n= 138; λ= 0.944) (Table 4). In this latter model, there was also a
weak positive effect of fission–fusion.
4. Discussion
Using scores for sexual dimorphism in ornamentation across simian
primates, we found that male ornamentation was greatest among pri-
mates living in larger social groups in single and multiple regressions
in phylogenetic models. Social organization was also associated with
male ornamentation, so that species living in multilevel social organiza-
tions, in which one-male units coalesce semi-permanently into bands,
scored highest for male ornamentation. However, no relationship to
habitat type (open or closed) or fission–fusion was found although
fission–fusion was weakly significant in model #4. Furthermore, scores
for sexually dimorphic visual traits were positively correlated with the
degree of sexual dimorphism in body mass, a finding that is consistent
with Dixson et al. (2005). However, female body mass was not related
to male ornamentation.
The studyof male ornaments as sociosexual signals has a long history
in primatology (Semple & Higham, 2013). Ornaments may act in concert
with behavioral displays to augment their value as signals to conspe-
cifics, particularly in large groups and modular societies wherein
animals regularly encounter unfamiliar individuals (sensu Maynard-
Smith, 1982). Positive correlations between group size and facial mobi-
lity were found among some non-human primates and may reflect
selection for more complex displays to reduce conflicts and enhance so-
cial bonding (Dobson, 2009). Positive relationships between group size,
sympatry with other primates, and the complexity of facial coloration
have also been reported for Old World monkeys and apes (Santana
et al., 2013) and among New World monkeys living in small social
groups with high levels of sympatry (Santana et al., 2012). Interestingly,
facial mobility is more developed among primates with less complex
facial coloration, suggesting a trade-off between ornamentation and
Fig. 1. Relationship between group size and visual trait dimorphism (both natural log transformed) in simian primates.
Table 3
Parameter estimates for phylogenetic generalized least squares regression model with
visual trait dimorphism as the response variable, group size as the main predictor and
social organization, fission–fusion, habitat, and female body mass as control predictors.
Predictor Level (for
factors)
Estimate Std
error
tp
Intercept 1.1496 0.7838 1.4668 0.1449
Ln group size 0.4106 0.0978 4.1994 b0.0001
Social
organization
mm-mf −1.2710 0.2938 −4.3255 b.00001
mm-sf −1.0447 0.4223 −2.4737 0.0147
sm-mf −1.0313 0.3455 −2.9847 0.0034
sm-sf −0.9381 0.4268 −2.1980 0.0297
Fission–fusion yes 0.1766 0.1712 1.0316 0.3042
Habitat open −0.0060 0.1963 −0.0304 0.9758
Ln ♀body mass 0.2851 0.2062 1.3827 0.1691
Lambda = 0.955. mm-mf = multimale–multifemale, mm-sf = multimale–singlefemale,
sm-mf = singlemale–multifemale.
5C.C. Grueter et al. / Evolution and HumanBehavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

signalling behavioral intent via facial expression (Santana, Dobson, &
Diogo, 2014).
In the present study we used a revised classification of social organiza-
tion and found the highest scores in species with multilevel social organi-
zations, followed by singlemale–multifemale, multimale–multifemale,
singlemale–singlefemale (these three being close together), and
multimale–singlefemale social organizations receiving a mean score of
zero. There are several examples of how large groups in combination
with multilevel social organizations might favor selection for augmented
conspicuous sexual signals of status. For example, geladas, hamadryas
baboons, and snub-nosed monkeys live in large bands composed of
smaller social units nested therein (Grueter, Chapais, et al., 2012;
Kirkpatrick & Grueter, 2010; Stammbach, 1987). Generally high scores
for visual trait dimorphism in these species support the prediction
that multilevel social organizations lead to the elaboration of ornamen-
tal features, possibly as a result of a relatively high potential for inter-
male competition (Grueter & van Schaik, 2009).
Our aim was to determine the extent to which social group size and
composition impact on variation in male primate ornamentation. How-
ever, previous research has shown that such sexual dimorphism in or-
namentation was greater in primate species with polygynous mating
systems, followed by monogamous and multimale–multifemale sys-
tems (Dixson et al., 2005). While we found that species with multilevel
social organizations received higher scores for ornamentation than
singlemale–multifemale groups, species from both these social organi-
zations, such as gorillas (singlemale–multifemale) and geladas (multi-
level) also have polygynous mating systems. One possibility is that
among geladas, where one-male units live in close proximity within a
multilevel society wherein males encounter one another frequently,
intra-sexual selection acts on visually conspicuous signals like the red-
ness of the chest (Bergman, 2010; Bergman et al., 2009). By contrast,
among gorillas one-male units are more widely spaced. However,
when social units interact the silvery grey chest and adipose crest size
function as visual signals of rank and dominance (Breuer et al., 2012,
Caillaud et al., 2008).
The male mandrill likely represents a special case for sexual selec-
tion acting on a suite of sexually dimorphic visually conspicuous traits
occurring on the genitalia, rump, body, and the face. Indeed, male man-
drills received the highest scores of ornamentation and have the largest
social groups sizes, but have multimale–multifemale social organiza-
tions. The larger female social groups were thought to segment into
smaller units that were suggested to be one-male polygynous units
(Barton, 2000), although studies in captivity reported that males mate
guard individual females but not harems of females (Dixson, Bossi, &
Wickings, 1993). However, studies tracking the movements and com-
positions of the large social groups comprised of hordes that number
up to 854 reveal that males join the social group during the breeding
season but likely do not remain in the social group, and instead depart
during the non-breeding season to live in isolation (Abernethy et al.,
2002). Thus, although we found strong effects of social group size and
social organization on male expressionof secondary sexualadornments,
in the case of the mandrill, these factors as they relate to the mating
system are complex.
Interestingly, theorang-utan does not conform to the pattern we ob-
served that primates living in large social groups express the most pro-
nounced ornamentation. With regards scores for male ornamentation,
the Bornean orang-utan (Pongo pygmaeus) received a high score of 22
and the Sumatran orang-utan (Pongo abelii) received a score of 18.
However, neither species form permanent social groups and males are
non-gregarious, occupying large home ranges that overlap with the
Fig. 2. Variation in visual trait dimorphism across different social organizations in simian primates. Filled circles represent species; species with the same values occupy the same space.
Table 4
Parameter estimates for phylogenetic generalized least squares regression model with
visual trait dimorphism as the response variable, group size as the main predictor and
mating system, fission-fusion, habitat, and female body mass as control predictors.
Predictor Level (for factors) Estimate Std error t p
Intercept 0.2638 0.7369 0.3580 0.7209
Ln group size 0.5280 0.0933 5.6590 b0.0001
Mating system Polyandrous −0.1442 0.2701 −0.5338 0.5944
Polygynous 0.0477 0.3196 0.1492 0.8816
promiscuous −0.4585 0.3038 −1.5094 0.1336
Fission–fusion yes 0.3392 0.1680 2.0192 0.0455
Habitat open 0.1330 0.1993 0.6670 0.5060
Ln ♀body mass 0.2087 0.2080 1.0033 0.3176
Lambda = 0.944.
6C.C. Grueter et al. / Evolution and Human Behavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

smaller individual home ranges of several females. Adult males engage in
“long calling”and “snag crashing”behaviors (the felling of trees and
branches), which may alert females of their location (Galdikas, 1983). Com-
pared to un-flanged males, flanged males achieve more matings when
females are at the peri-ovulatory phase of their menstrual cycles (Knott
et al., 2010) and have higher reproductive success than un-flanged males
(Utami Atmoko & van Hooff, 2004). Thus, although male orang-utans rarely
meet, they are highly competitive and antagonistic, which may have
shaped their pronounced visual and vocal signals of status.
Gradation in visual signals reflects status and quality in some of the
more conspicuously adorned primate species such as mandrills, geladas,
and orang-utans (Bergman et al., 2009; Setchell & Dixson, 2001a; Utami
Atmoko & van Hooff, 2004). However, whether such gradation in orna-
ments occurs among other primates remains less well known. Thus,
traits such as the beards of howler monkeys, ‘proboscides’in proboscis
monkeys, capes of hair in hamadryas baboons, and facial coloration in
snub-nosed monkeys have not been systematically investigated. At
present it also remains unknown to what extent these male ornaments
exhibit within-species variation in their expression. Future studies
quantifying variation within males in such ornamental traits would
therefore be valuable.
Berglund, Bisazza, and Pilastro (1996) proposed that male–male
competition is a stronger selective force acting on male ornaments
than female choice, which may have emerged as a secondary selective
factor. A similar argument has also been made for how sexual selection
has shaped men's secondary sexual traits (Puts, 2010). While men lack
the pronounced canines that characterize high levels of male–male
competition in other primates (Plavcan, 2012), sexual dimorphism in
muscularity, craniofacial shape, and beards could play analogous roles
in same-sex competition as signals of dominance that secondarily influ-
ence attractiveness (Dixson, Grimshaw, Ormsby, & Dixson, 2014; Puts,
2010; Scott, Clark, Boothroyd, & Penton-Voak, 2013). Thus, beards
receive higher ratings for facial aggressiveness, age, masculinity, and so-
cial dominance, but not attractiveness compared with clean-shaven
faces (Dixson & Brooks, 2013; Dixson, Tam, & Awasthy, 2013; Dixson
& Vasey, 2012; Muscarella & Cunningham, 1996; Neave & Shields,
2008). While male patterned baldness may also lower men's attractive-
ness, it augments ratings of men's age, masculinity, and aspects of non-
threatening social dominance (Muscarella & Cunningham, 1996).
Although beards and baldness do not aid directly in fighting, they
could signal of masculinity, age, and dominance that curtail agonistic in-
teractions from escalating into costly fights. Success in intra-sexual
competition can determine detection rates of high quality mates and re-
sult in direct benefits such as resources and territory quality (Wong &
Candolin, 2005). Among Hadza hunter-gatherers, men with physically
stronger upper-bodies had greater reproductive success and were
most likely to be nominated as better hunters by women (Apicella,
2014). Thus, like male nonhuman primates men's secondary sexual
traits may have evolved primarily under intra-sexual selection and
secondarily influence their attractiveness to women.
The origins of human social organizations likely reflect more closely
those found in contemporary hunter–gather societies, wherein social
networks were comprised of closely related kin and individual recogni-
tion of group members was high (Apicella, Marlowe, Fowler, &
Christakis, 2012). However, the pronounced social integration within
contemporary societies (Grueter & White, in press) coupled with their
larger group sizes and greater ‘anonymity’(Moffett, 2013), may also
act as a strong selective force for the display of male ornaments associa-
ted with age, dominance and attractiveness. For example, while beards
are androgen-dependent secondary sexual traits, their signalling is
strongly culturally determined (Reynolds, 1949)andsubjecttotempo-
ral variation (Barber, 2001). Interestingly, the popularity of styles of
moustaches and beardedness among British men from 1842 to 1971
rose when there were more males in potential marriage pool (Barber,
2001), and beards are judged to be more attractive when beards are
rare relative to clean-shaven faces (Janif, Brooks, & Dixson, 2014).
Cultural cues of intra-sexual status may also aid in the recognition of
allies, indicate group membership, and delineate a parochial group
against out-groups (McElreath, Boyd, & Richerson, 2003;Moffett,
2013). Future research exploring how variation in social cues of status
predicts male attractiveness cross-culturally would be valuable.
A limitation of the present study was the use of relatively crude and
somewhat subjective Likert-type scales to quantify the degree of sexual
dimorphism in male ornamentation. We also relied on photographs
wherein lighting conditions varied, which may have impacted on the
accuracy of the degree of sexual dimorphism in colorful traits. We there-
fore see potential for follow-up studies that may replicate the analyses
with a more fine-grained, quantitative, and overall objective measures
of color and form of signals (Allen & Higham, 2013). Future analyses
may also benefit from taking into account variation in primate visual
systems, as coloration and conspicuousness may differ depending on
the receiver's visual system (Stevens, Stoddard, & Higham, 2009). We
were primarily interested in characterizing the magnitude of variation
in sexual dimorphismin visually conspicuous traits as they occur across
primates with different social organizations. Thus, we did not characte-
rize variation in sexually monomorphic traits as they relate to environ-
mental factors. Himalayan Hanuman langurs (Semnopithecus entellus),
for example, are thought to have longer and thicker coats as an adapta-
tion to cold winter, which may explain why both sexes invest in this
trait. Other cases where both males and females display ornamental fea-
tures and no thermoregulatory benefits, such as the bright pink lips of
black-and-white snub-nosed monkeys or prominent beards in black
colobus monkeys, require alternative explanations. For the present,
our study provides strong preliminary support for the effect of group
size on sexually selected visual signals in primates, which may reflect
enhanced selective pressures acting on signals of social status or attrac-
tiveness to conspecifics in crowded social organizations.
Acknowledgments
We are very grateful to Professor Alan Dixson for supplying details
regarding the data and descriptions of sexually dimorphic traits that
formed the majority of the data reported here. We are also grateful to
Dr Quentin Atkinson and three anonymous reviewers for their thoughtful
comments on earlier drafts of our manuscript.
References
Abernethy, K. A., White, L. J. T., & Wickings, E. J. (2002). Hordes of mandrills (Mandrillus
sphinx): Extreme group siz e and seasonal male presence. Journal of Zoology,258,
131–137.
Allen, W. L., & Higham, J. P. (2013). Analyzing visual signals as visual scenes. American
Journal of Primatology,75,664–682.
Allen, W. L.,Stevens, M., & Higham,J. P. (2014). Character displacement of Cercopithecini
primate visual signals. Nature Communications,5,4266.
Andersson, M. (1994). Sexual selection. Princeton: Princeton University Press.
Apicella, C.L. (2014). Upper-body strength predicts hunting reputation and reproductive
success in Hadza hunter–gatherers. Evolution and Human Behavior,35,508–518.
Apicella,C. L., Marlowe, F. W., Fowler, J. H., & Christakis, N. A. (2012). Social networks and
cooperation in hunter-gatherers. Nature,481,497–501.
Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., et al. (2008).
Fission–fusion dynamics: New research frameworks. Current Anthropology ,49,
627–654.
Barber, N. (2001). Mustache fashion covaries with a good marriage market for women.
Journal of Nonverbal Behavior,25,261–272.
Barrette, C., & Vandal, D. (1990). Sparring, relative antler size, and assessment in male
caribou. Behavioral Ecology and Sociobiology,26,383–387.
Barton, R. A. (2000). Socioecology of baboons: The interface of male and f emale strategies. In P.
M. Kappeler (Ed.), Primate Males (pp. 97–107). Cambridge: Cambridge University Press.
Berglund, A., Bisazza, A., & Pilastro, A. (1996). Armaments and ornaments: An evolutionary
explanationof traits of dualutility.Biological Journal of the Linnean Society ,58,385–399.
Bergman, T. J. (2010). Experimental evidence for limited vocal recognition in a wild pri-
mate: Implications for the social complexity hypothesis. Proceedings of the Royal
Society of London. Se ries B,277,3
045–3053.
Bergman, T. J., Ho, L., & Beehner, J. C. (2009). Chest color and social status in male geladas
(Theropithecus gelada). International Journal of Primatology,30,791–806.
Bergman, T. J., & Sheehan, M. J. (2013). Social knowledge and signals in primates.
American Journal of Primatology,75,683–694.
7C.C. Grueter et al. / Evolution and HumanBehavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

Bradley,B. J., & Mundy, N. I. (2008). The primate palette: The evolution of primate colora-
tion. Evolutionary Anthropology,17,97–111.
Breuer, T., Robbins, A. M., Boesch, C., & Robbins, M. M. (2012). Phenotypic correlates of male
reproductive success in western gorillas. Journal of Human Evolution,62, 466–472.
Caillaud, D., Levréro, F., Gatti, S., Ménard, N., & Raymond, M. (2008). Influence of male
morphology on male mating status and behavior during interunit encou nters in
western lowland gorillas. American Journal of Physical Anthropology,135,379–388.
Campbell, C. J., Fuentes, A., MacKinnon, K. C., Bearder, S. K., & Stumpf, R. M. (2011).
Primates in perspective (2nd ed.). Oxford: Oxford University Press.
Chaplin, G., & Jablonski, N. G. (1998). The integument of the “odd-nosed”colobines. In N. G.
Jablonski (Ed.), The natural history of the doucs and snub-nosed monkeys.Singapore:
World Scientific Press.
Darwin, C. (1871). The descent of man, and selection in relation to sex. London: John Murray.
Dixson, A. F. (1987). Observations on the evolution of the genitalia and copulatory behaviour
in male primates. Journal of Zoology,213, 423–443.
Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys,
apes, and human beings. Oxford University Press.
Dixson, A. F., Bossi, T., & Wickings, E. J. (1993). Male dominance and genetically deter-
mined reproductive success in the mandrill (Mandrillus sphinx). Primates,34,
525–532.
Dixson, B.J., & Brooks, R. C. (2013).The role of facial hair in women's perceptionsof men's
attractiveness, health, masculinity and parenting abilities. Evolution and Human
Behavior,34,236–241.
Dixson, A. F., Dixson, B. J., & Anderson, M. (2005). Sexual selection and the evolution of
visually conspicuous sexually dimorphic traits in male monkeys, apes, and human
beings. Annual Review of Sex Research,16,1–19.
Dixson, B.J., Grimshaw, G. M., Ormsby, D. K., & Dixson, A. F. (2014). Eye-tracking women's
preferences for men's somatotypes. Evolution and Human Behavior,35,73–79.
Dixson, B. J., Tam, J. C., & Awasthy, M. (2013). Do women's preferences for men's facial
hair change with reproductive status? Behavioral Ecology,24,708–716.
Dixson, B. J., & Vasey, P. L.(2012). Beards augment perceptions of men's age, social status,
and aggressiveness, but not attractiveness. Behavioral Ecology,23,481–490.
Dobson, S. D. (2009). Socioecological correlates of facial mobility in nonhuman anthro-
poids. American Journal of Physical Anthropology,139,413–420.
Dubuc, C.,Allen, W. L., Maestripieri, D., & Higham, J. P. (2014). Is male rhesusmacaque red
color ornamentation attractive to females? Behavioral Ecology and Sociobiology,68,
1215–1224.
Endler, J. A. (2000). Evolutionary implications of the interaction between animal signals
and the environment. In Y. Espmark, T. Amundsen, & G. Rosenquist (Eds.), Animal
signals: Signa lling and design in anima l communication (pp. 11–46). Trondheim:
Tapir Academic.
Galdikas, B. M. (1985). Adult malesociality and reproductive tactics among orangutans at
Tanjung Puting. Folia Primatologica,45,9–24.
Galdikas, B. M. F. (1983). The orangutan long call and snag crashing at Tanjung Puting Re-
serve. Primates,24,371–384.
Grueter, C. C. (2009). Determinants of modular societies in snub-nosed monkeys
(Rhinopithecus bieti) and other Colobines. [Ph.D. dissertation] Zurich, Switzerland:
University of Zurich.
Grueter, C. C. (2013). The biology of the snub-nosed monkeys, douc langurs, proboscis mon-
keys and simakobu. Hauppauge, NY: Nova.
Grueter, C. C., Chapais, B., & Zinner, D. (2012a). Evolution of multilevel social systems in
nonhumanprimates and humans. InternationalJournal of Primatology,33,1002–1037.
Grueter, C. C., Matsuda, I., Zhang, P., & Zinner, D. (2012b). Multilevel societies in primates
and other mammals: Introduction to the special issue. Intern ational Journal of
Primatology,33,993–1001.
Grueter, C. C., & van Schaik, C. P. (2009). Sexual size dimorphism in Asian colobines
revisited. American Journal of Primatology,71,609–616.
Grueter, C.C., & White, D. in press. On the emergence of large-scale humansocial integra-
tion and its antecedants in primates. Structure and Dynamics: eJournal of Anthropo-
logical and Related Sciences.
Grueter, C. C., & Zinner, D. (2004). Nested societ ies. Convergent adaptations in snub-
nosed monkeys and baboons? Primate Report,70,1–98.
Harcourt, A. H., & Gardiner, J. (1994). Sexual se lection and genital anatomy of male
primates. Proceedings of the Royal Society of London. Series B,255,47–53.
Houde, A. E. (1997). Sex, color and mate choice in guppies. Princeton, NJ: Princeton
University Press.
Isler, K., Kirk, E. C., Miller, J. M. A., Albrecht, G. A., Gelvin, B. R., & Martin, R. D. (2008).
Endocranial volumes of primate species: Scaling analyses using a comprehensive
and reliable data set. Journal of Human Evolution,55,967–978.
Janif, Z. J., Brooks, R. C., & Dixson, B. J. (2014). Negative frequency-dependent preferences
and variation in male facial hair. Biology Letters,10, 20130958.
Kamilar, J. M., & Bra dley, B. J. (2011). Interspecific variat ion in primate coat colour
supports Gloger's rule. Journal of Biogeography,38, 2270–2277.
Kappeler,P. M., & van Schaik, C. P. (2004). Sexualselection in primates: review and selective
preview. Sexual selection in primates: new and comparative perspectives. New York:
Cambridge University Press, 3–23.
Kingsley,S. (1982). Causes of non-breeding and the development of the secondary sexual
characteristics in the male orang-utan: A hormonal study. In L. E. M. de Boer (Ed.),
The orang-utan: it s biology and conservation (pp. 215–229). The Hague (The
Netherlands): Junk Publishers.
Kirkpatrick, R. C., & Grueter, C. C. (2010). Snub-nosed monkeys: Multilevel societiesacross
varied environments. Evolutionary Anthropology,19,98–113.
Knott, C. D., Thompson, M. E., Stumpf, R. M., & McIntyre, M. H. (2010). Female reproduc-
tive strategies in orangutans, evidence for female choice and counterstrategies to in-
fanticide in a species with frequent sexual coercion. Proceedings of the Royal Society B,
277,105–113.
Layton, R., & O'Hara, S. (2009). Human social evolution: A comparison of hunter-gatherer
and chimpanzee social organization. In R. Dunbar, C. Gamble, & J. Gowlett (Eds.),
Social Brain, Distributed Mind (pp. 83–114). Oxford: Oxford University Press.
Marchetti,K. (1993). Dark habitats and bright birds illustrate the role of the environment
in species divergence. Nature,362,149–152.
Marty, J.S., Higham, J. P., Gadsby, E. L., & Ross, C. (2009).Dominance, coloration, and social
and sexual behavior in male drills Mandrillus leucophaeus.Internatio nal Journal of
Primatology,30,807–823.
Maynard-Smith, J. (1982). Evolution and the theory of games. Cambridge Press: Cambridge
University.
McElreath, R., Boyd, R.,& Richerson, P. J. (2003). Shared norms and the evolution of ethnic
markers. Current Anthropology,44,122–129.
Mittermeier, R. A., Rylands, A. B., & Wilson, D. E. (Eds.). (2013). Handbook of the mammals
of the world. Primates,Vol. 3,.Barcelona:LynxEdicions.
Moffett, M. W. (2013). Human identity and the evolution of societies. Human Nature,24,
219–267.
Muscarella, F., & Cunningham, M. R. (1996). The evolutionary significance and social percep-
tion of male pattern baldness and facial hair. Ethology and Sociobiology,17,99–117.
Neave, N., & Shields, K. (2008). The effects of facial hair manipulation on female percep-
tions of attractiveness, masculinity, and dominance in male faces. Personality and
Individual Differences,45,373–377.
Nunn, C. L. (2011). The comparative approach in evolutionary anthropology and biology.
Chicago: The University of Chicago Press.
Nunn, C. L., & Altizer, S. (2006). Infect ious diseases in prima tes: Behavior, ecolog y and
evolution. Oxford: Oxford University Press.
Orme, D., Freckleton, R. P., Thomas, G., Petzoldt, T., & Fritz, S. A. (2011). Caper: Comparative
analyses of phylogenetics and evolution in R. (http://r-forge.r-project.org/projects/caper).
Perelman,P., Johnson, W. E., Roos, C., Seua´nez,H. N., Horvath, J. E., Moreira, M. A. M.,et al.
(2011). A molecular phylogeny of living primates. PLoS Genetics,7, e1001342.
Plavcan, J. M. (2012). Sexual size dimorphism, canine dimorphism , and male–male
competition in primates. Human Nature,23,45–67.
Plavcan, J. M.,& van Schaik, C. P. (1992). Intrasexual competition and canine dimorphism
in anthropoid primates. American Journal of Physical Anthropology,87,461–477.
Plavcan, J.M., & van Schaik, C. P. (1997). Intrasexual competition and bodyweight dimor-
phism in anthropoid primates. American Journal of Physical Anthropology,103,37–68.
Puts, D. A. (2010). Beauty and the beast: Mechanisms of sexual selection in humans.
Evolution and Human Behavior,31,157–175.
R Develpopment Core Team (2012). R: A language and environment for statistical computing.
Vienna, Austria: R Foundation for Statistical Computing.
Reynolds, R. (1949). Beards: Their social standing religious involvements, decorative
possibilities, and value in offence and defence through the ages. New York: Harcourt
Brace Jovanovich.
All the World's Primates. Rowe, N., & Myers, M. (Eds.). (2011). Charlestown RI: Primate
Conservation Inc (www.alltheworldsprimates.org).
Santana, S. E., Alfaro, J. L., & Alfaro, M. E. ( 2012). Adaptive evolution of facial colour
patterns in Neotropical primates. Proceedings of the Royal Society B,279,2204–2211.
Santana,S. E., Alfaro, J. L., Noonan, A., & Alfaro, M. E. (2013).Adaptive response to sociality
and ecology drives the diversification of facial colour patterns in catarrhines. Nature
Communications,4,2765.
Santana, S. E., Dobson, S. D., & Diogo, R. (2014). Plain faces are more expressive: comparative
study of facial colour, mobility and musculature in primates. Biology Letters,10,
20140275.
Scott, I. M., Clark, A. P., Boothroyd, L. G., & Penton-Voak, I. S. (2013). Do men's faces really
signal heritable immunocompetence? Behavioral Ecology,24,579–589.
Semple,S.,&Higham,J.P.(2013).Primate signals: Current issues and perspectives.
American Journal of Primatology,75,613–620.
Setchell,J. M., Charpentier, M. J. E., Abbott, K. M., Wickings, E. J., & Knapp, L. A. (2010).Op-
posites attract: MHC-associated mate choice in a poly gynous primate. Journal of
Evolutionary Biology,23,136–148.
Setchell, J. M., & Dixson, A. F. (2001a). Changes in the secondary sexual adornments of
male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status.
Hormones and Behavior,39,177–184.
Setchell, J. M., & Dixson, A. F. (2001b). Arrested development of secondary sexual adorn-
ments in subordinate adult male mandrills (Mandrillus sphinx). American Journal of
Physical Anthropology,115,245–252.
Setchell, J. M., & Hu chard, E. (2010). The hidden benefits of sex: Evide nce for MHC-
associated mate choice in primate societies. Bioessays,32,940–948.
Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to sex in primates. Advances
in the Study of Behavior,33,87–174.
Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of
Human Evolution,32,523–559.
Snaith,T.V.,&Chapman,C.A.(2008).Red colobus monkeys display alternative behavioral
responses to the costs of scramble competition. Behavioral Ecology,19,1289–1296.
Stammbach, E. (1987). Desert, forest and montane baboons: Multilevel-societies. In B. B.
Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsake r (Eds.),
Primate Societies (pp. 112–120). Chicago: University of Chicago Press.
Stevens, M., Stoddard, M. C., & Higham, J. P. (2009). Studying primate color: Towards visual
system-dependent methods. International Journal of Primatology,30, 893–917.
Stoinski, T. S., Rosenbaum,S., Ngaboyamahina, T., Vecellio,V., Ndagijimana,F., & Fawcett, K.
(2009). Patterns of male reproductive behaviour in multi-male groups of mountain
gorillas: examining theories of reproductive skew. Behaviour,146,1193–1215.
Stuart–Fox, D. M., & Ord, T. J. (2004). Sexual selection, natural selection and the evolution
of dimorphiccoloration and ornamentationin agamid lizards. Proceedings of the Royal
Society of London,271,2249–2255.
Utami Atmoko,S., & van Hooff, J. A. R. A. M. (2004). Alternative reproductive tactics: Male
bimaturism in orangutans. In P. Kappeler, & C. van Schaik (Eds.), Sexual selection in
8C.C. Grueter et al. / Evolution and Human Behavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003

primates: New and comparative perspectives (pp. 196–207). Cambridge (UK):
Cambridge University Press.
van Schaik, C. P., & van Hooff, J. A. R. A. M. (1996). Towards an understanding of the
orangutan's social system. In W. C. McGrew, L. F. Mar chant, & T. Nishida (Eds.),
Great ape societies (pp. 3–15). Cambridge: Cambridge University Press.
Verrell, P. A. (1992). Primate penile morphologies and social systems: Further evidence
for an association. Folia Primatologica,59,114–120.
Wickings, E. J., & Dixson, A. F. (1992). Testicular function, secondary sexual development,
and social status in male mandrills (Mandrillus sphinx). Physiology & Behavior,52,
909–916.
Willems, E. P., Hellriegel, B., & van Schaik, C. P. (2013). The collective action problem in
primate territory economics. Proceedings of the Royal Society B,280, 20130081.
Wong, B., & Candolin, U. (2005). Howisfemalematechoiceaffectedbymalecompetition?
Biological Reviews,80, 559–571.
9C.C. Grueter et al. / Evolution and HumanBehavior xxx (2015) xxx–xxx
Please cite this article as: Grueter, C.C., et al., Are badges of status adaptive in large complex primate groups?, Evolution and Human Behavior
(2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.03.003