YEARBOOK OF PHYSICAL ANTHROPOLOGY 44:2553 (2001)

Sexual Dimorphism in Primate Evolution

J. Michael Plavcan

Department of Anthropology, University of Arkansas, Fayetteville, Arkansas 27701

KEY WORDS sexual dimorphism; sexual selection; canine teeth; primates

ABSTRACT Sexual dimorphism is a pervasive phe-
nomenon among anthropoid primates. Comparative anal-
yses over the past 30 years have greatly expanded our
understanding of both variation in the expression of di-
morphism among primates, and the underlying causes of
sexual dimorphism. Dimorphism in body mass and canine
tooth size is familiar, as is pelage and sex skin dimor-
phism. More recent analyses are documenting subtle dif-
ferences in the pattern of skeletal dimorphism among
primates. Comparative analyses have corroborated the
sexual selection hypotheses, and have provided a more
detailed understanding of the relationship between sexual
selection, natural selection, and mating systems in pri-
mates. A clearer picture is emerging of the relative con-
tribution of various selective and nonselective mecha-
nisms in the evolution and expression of dimorphism.
Most importantly, recent studies have shown that dimor-
phism is the product of changes in both male and female
traits. Developmental studies demonstrate the variety of
ontogenetic pathways that can lead to dimorphism, and
provide additional insight into the selective mechanisms
that influence dimorphism throughout the lifetime of an
animal. Evidence from the fossil record suggests that di-
morphism probably evolved in parallel twice, and the di-
morphism in some extinct hominoids probably exceeded
that of any living primate. Our advances in understanding
the behavioral/ecological correlates of dimorphism in liv-
ing primates have not improved our ability to reconstruct
social systems in extinct species on the basis of dimor-
phism alone, beyond the inference of polygyny or intense
male-male competition. However, our understanding of
the behavioral/ecological correlates of growth and devel-
opment, and of the expression of dimorphism as a function
of separate changes in male and female traits, offers great
potential for inferring evolutionary changes in behavior
over time.Yrbk Phys Anthropol 44:2553, 2001.
2001 Wiley-Liss, Inc.

TABLE OF CONTENTS

Variation in Dimorphism in Primates ..................................................................................................................... 26

Definitions .............................................................................................................................................................. 26
Primary sex differences ......................................................................................................................................... 26
Secondary sex differences ..................................................................................................................................... 27
Body mass dimorphism ..................................................................................................................................... 27
The canine/premolar complex ........................................................................................................................... 27
Dental and skeletal dimorphism ...................................................................................................................... 29
Pelage and skin dimorphism ............................................................................................................................. 32
Causal Models ........................................................................................................................................................... 32
Sexual selection ..................................................................................................................................................... 32
History of comparative studies of dimorphismsexual selection vs. other mechanisms ............................ 33
Recent models of mate competition, intrasexual competition, and dimorphism .......................................... 36
Sperm competition ............................................................................................................................................. 38
Mate choice ......................................................................................................................................................... 39
Models for other causes of dimorphism ............................................................................................................... 40
Body size ............................................................................................................................................................. 40
Diet ...................................................................................................................................................................... 41
Terrestriality ...................................................................................................................................................... 42
Correlated response ........................................................................................................................................... 42
Niche divergence ................................................................................................................................................ 43
Taxonomy ........................................................................................................................................................... 43
Epiphenomenal variation .................................................................................................................................. 44
Ontogeny .................................................................................................................................................................... 44
Dimorphism in the Fossil Record ............................................................................................................................ 46
Dimorphism in the primate fossil record ............................................................................................................. 46

2001 WILEY-LISS, INC.

DOI 10.1002/ajpa.10011
26 YEARBOOK OF PHYSICAL ANTHROPOLOGY
Dimorphism in hominids ...................................................................................................................................... 48
Conclusions ................................................................................................................................................................ 49
Acknowledgments ...................................................................................................................................................... 49
Literature Cited ........................................................................................................................................................ 50
Sexual dimorphism is a common phenomenon
among living and extinct primates. The past several
decades have seen a steady growth in studies of
dimorphism, ranging from simple documentation of
the phenomenon in various species to broad compar-
ative analyses incorporating humans and a wide
variety of primates. Consequently, our understand-
ing of the expression, evolution, and development of
sexual dimorphism in primates and humans has
increased dramatically.
This essay reviews recent advances in our under-
standing of the expression and evolution of dimor-
phism across primates. However, it should be kept
in mind that anthropologists and primatologists are
interested in sexual dimorphism for a variety of
reasons. Forensic anthropologists seek characters
that allow accurate sex identification on the basis of
skeletal and dental remains. Human biologists are
interested in sexual dimorphism as a component of
population variation, and what it reveals about
health and epiphenomenal adaptation in local pop-
ulations. Systematists, morphologists, and paleon-
tologists need to understand sexual dimorphism as a
component of trait variation, either as a species-
specific character, or as a component of variation
that needs to be distinguished from potential inter-
specific character variation. Dimorphism can also
offer evidence about the behavior of extinct species.
Primate biologists are interested in understanding
the causes of sexual dimorphism in primates, and
how these relate to variation in behavior and ecology
(e.g., Crook, 1972; Leutenegger and Kelly, 1977; Ox-
nard, 1987; Plavcan and van Schaik, 1994; Leigh
and Shea, 1995).
Most comparative analyses address two basic ques-
tions: what are the differences and similarities in the
ways that dimorphism is expressed among species,
and what are the causes of variation in the magnitude
and pattern of dimorphism among species? In this
essay, I review recent advances in answering these
two questions. I shall first survey dimorphism among
primates, focusing particularly on variation in the ex-
pression of dimorphism. Next, I shall evaluate compar-
ative models of the causes of sexual dimorphism in
primates, including a discussion of sexual selection
and behavioral ecological models of dimorphism, and
the relation between life-history, ontogeny, and dimor-
phism. Finally, I provide a brief survey of dimorphism
in the fossil record and discuss whether it can be used
to reconstruct behavior.
VARIATION IN DIMORPHISM IN PRIMATES
Definitions
Biologists recognize two basic types of dimorphic
characters: primary sex differences and secondary
[Vol. 44, 2001
sex differences. Primary sex differences are those
directly related to mating and reproduction, includ-
ing obstetrically related differences in the pelvis.
Secondary sex differences are any other differences
not directly related to mating. Primary sex differ-
ences are not often referred to as dimorphic char-
acters (though there is nothing wrong with doing
so). Rather, the term sexual dimorphism is usually
reserved for secondary sex differences, particularly
if they are thought to arise from sexual selection
(Crook, 1972). However, the term is sometimes used
with reference to any sexual difference, including
genetic and biochemical differences. For example,
platyrrhine monkeys have sexually dimorphic al-
leles for color vision (Jacobs, 1994), while Gustafs-
son (1994) discusses metabolic liver dimorphism in
rats.
Primary sex differences
Primary sex differences are not commonly consid-
ered in discussions of the evolution of primate sex-
ual dimorphism, but it is worth noting that the
genitalia of primates can differ substantially in form
among species (Hershkovitz, 1977; Fooden, 1980;
Dixson, 1987; Harcourt and Gardiner, 1994; Har-
court, 1995; Verrell, 1992). For example, most male
primates have a bone (the baculum) in the penis
which differs in form and size among species. The
baculum is lacking in Ateles, Lagothrix, Brachyteles,
Chiropotes, Tarsier, and Homo (Hershkovitz, 1977).
Penile morphology is highly variable (Hershkovitz,
1977; Harcourt and Gardiner, 1994; Harcourt,
1995). Generally, strepsirrhines tend to have spines
on the penis, while most anthropoids do not (Har-
court and Gardiner, 1994). Within these groups,
though, even closely related species can differ sub-
stantially in penile morphology. Scrotal morphology
is also variable, but to a lesser degree than penile
morphology. Relative testicular volume also varies
among species (Harcourt, 1995), as does the size of
the seminal vesicles (Dixson, 1997).
There is also a wide variation in the external
appearance of the female genitalia: the labial folds,
clitoris, and associated structures, even among
closely related species (Le Gros Clark, 1971; Hersh-
kovitz, 1977). Additionally, the skin in and around
the genital area varies widely among primates in
cyclical changes associated with the menstrual cycle
(though this is usually considered a secondary sex
characteristic). Such sex-skins have evolved at
least three times among catarrhine primates, and
are found in species of Pan, Colobus, Procolobus,
Papio, Macaca, Cercocebus, Lophocebus, Mandril-
lus, Theropithecus (swellings located on the chest),
Miopithecus, and Allenopithecus. (Crook, 1972; Pa-
gel, 1994; van Schaik et al., 1999; Nunn, 1999).
J.M. Plavcan] DIMORPHISM IN PRIMATES 27
These vary among species in size, shape, and dura-
tion.
The reasons for most interspecific variation in
genital morphology are unclear (Harcourt and
Gardiner, 1994; Harcourt, 1995). Sexual selection,
the common explanation for sexual dimorphism in
primates, probably plays little role in most variation
of the scrotum, penis, baculum, clitoris, labia, and
associated structures (Harcourt and Gardiner, 1994;
Harcourt, 1995). Some genital differences are
thought to function as a reproductive isolating
mechanism: variation in genital morphology can cre-
ate a lock-and-key morphology discouraging
closely related species from interbreeding. Such spe-
cies-specific variation can be useful for alpha taxon-
omy (e.g., Fooden, 1980). However, Le Gros Clark
(1971) notes that genital variation is so great, even
among closely related species, as to be useless for
higher taxonomic studies. There has been a great
deal of discussion of the evolutionary mechanisms
underlying variation in testicular volume (Dixson,
1987; Verrell, 1992; Harcourt, 1995), and in the ex-
aggerated perineal swellings of female catarrhines
(Harcourt, 1995; van Schaik et al., 1999; Nunn,
1999; Stallmann and Froehlich, 2000). These are
discussed below in the section on sexual selection.

Secondary sex differences
Secondary sex differences are highly variable in
expression among primates, and are sometimes
spectacular. For the most part, secondary sex differ-
ence are confined to the anthropoid primates; strep-
sirrhine primates and tarsiers are, with a few excep-
tions, monomorphic. The most obvious secondary
sex differences among primates are body mass di-
morphism, and canine tooth size dimorphism. Skel-
etal dimorphism is often pronounced in primates,
and is primarily a product of body mass dimorphism
(Fig. 1). Pelage dimorphism, while not pervasive
among primates, is present in several species and
can be quite impressive. Table 1 summarizes the
distribution of dimorphism among primates.
Body mass dimorphism. In most anthropoid pri-
mates, males are larger than females. The most
extremely size-dimorphic primates are gorillas, or-
angutans, mandrills, baboons, and proboscis mon-
keys, with males sometimes more than twice as
large as females (Crook, 1972; Clutton-Brock et al.,
1977; Leutenegger and Kelly, 1977; Plavcan and van
Schaik, 1997b; Smith and Jungers, 1997). Most cer-
copithecoid male primates range from about 30
80% larger than females in body mass. Body mass
differences between males and females are often
characterized as species-specific traits, but there is
good evidence for biologically meaningful subspecific
variation in body mass dimorphism in some species
(Turner et al., 1994, 1997; Smith and Jungers, 1997;
Plavcan and van Schaik, 1997b; Jones et al., 2000).
Fig. 1. Illustration of lateral views of male and female Ma-
caca fascicularis skulls. This species shows typical dimorphism
for a cercopithecoid primate. Note magnitude of size difference
between male and female skulls, somewhat greater robusticity of
the skull, longer male face, and much larger male canine.
Reverse dimorphism 1 is only characteristic of
some callitrichine primates and possibly some strep-
sirrhines (Kappeler, 1990, 1991; Godfrey et al.,
1993; Plavcan and van Schaik, 1997b). In general,
body mass dimorphism reaches its extremes in
hominoids and papionines. Platyrrhines on the
whole are characterized by lesser degrees of body
mass dimorphism, though there are a few species
(howler monkeys) that are comparable to cercopithe-
coids (Ford, 1994; Plavcan and van Schaik, 1997b).
The canine/premolar complex. Canine tooth
size dimorphism is also common in anthropoids
(Crook, 1972; Leutenegger and Kelly, 1977; Harvey
et al., 1978; Plavcan and van Schaik, 1992, 1994).
The maxillary canine teeth tend to be more dimor-
phic than the mandibular canines. Cercopithecoid
male canine teeth tend to be very long and dagger-
like, and can be up to 400% taller than those of
1
The term reverse dimorphism is used to indicate that females are
larger than males. Some object to this term as sexist, reflecting male
bias in primatology. However, in primates almost all species have
males larger than females. Dimorphism is usually expressed quanti-
tatively as a ratio of the larger sex to the smaller (the opposite practice
is statistically inadvisable), meaning that ratios reflect male values
divided by female values. Reverse dimorphism is used to indicate that
the opposite relation is true.
 TABLE 1. Summary of body mass, canine tooth size, and pelage dimorphism in primates1
Taxon Body mass dimorphism Canine dimorphism Pelage and other dimorphisms

Lorisids Slight reverse to moderate Slight None

Galagids Slight to moderate Slight to moderate None
Lemurids Reverse to none Slight to moderate Most, none; Lemur macaco,
dichromatic
Cheirogalids Slight reverse to moderate None None
Indriids Slight reverse None None
Lepilemurids None Slight to moderate None
Daubentonia None None None
Tarsier None None None
Callitrichines None, females sometimes slightly None None
larger than males
Aotus None None None
Saimiri Moderate; males gain weight during Moderate None
breeding season
Cebus Slight Slight; female canines relatively None
large
Callicebus None None None
Pithecia Slight Slight; female canines relatively P. pithecia dichromatic
large
Cacajao Slight Slight; female canines relatively None
large
Chiropotes Slight Slight; female canines relatively None
large
Ateles Moderate Moderate None
Brachyteles None None None
Lagothrix Moderate Moderate None
Alouatta Strong Strong A. caraya dichromatic; males
have enlarged hyoid bone
Cercopithecus Moderate to strong Moderate to strong; female canines Most have none; some have
relatively large different colors on genital
skin
Allenopithecus Strong Strong Females with exaggerated
estrous swellings
Miopithecus Strong Strong Females with exaggerated
estrous swellings
Erythrocebus Strong Extreme None
Lophocebus Strong Strong Females with exaggerated
estrous swellings
Cercocebus Strong Strong Females with exaggerated
estrous swellings
Macaca Moderate to strong Strong to extreme Females with exaggerated
estrous swellings in some
species (M. fascicularis,
nemestrina)
Papio Strong to extreme Extreme Females with exaggerated
estrous swellings; male P.
hamadryas and P. papio
have mane
Mandrillus Extreme Extreme Females with exaggerated
estrous swellings; male
mandrills with brilliant
facial and perianal colors;
less brightly colored facial
display in drills
Theropithecus Extreme Extreme Males with large mane and lip
display; females with
brilliant chest and
abdominal sexual skin;
males have lesser developed
homologous sex skins
Colobus Slight to moderate Strong; guereza females have None
relatively large canines
Procolobus Moderate Strong Females with exaggerated
estrous swellings
Presbytis Slight Slight to strong None
Trachypithecus Moderate Strong None
Semnopithecus Moderate Strong None
Kasi Moderate Strong None
Nasalis Strong Strong Males with bulbous nose
Simias Strong Strong None
Rhinopithecus Strong Strong None
Pygathrix Strong Strong None
Hylobates Slight Slight H. concolor, hoolock, and
pileatus dichromatic; male
gibbons have enlarged
hyoid bones
Pan Moderate Moderate Females with exaggerated
perianal swellings
Gorilla Extreme Strong Older males develop silver
back hair
Pongo Extreme Strong Older males with gular
pouches, cheek flanges
Homo Moderate Slight Males with facial and body
hair; females with enlarged
breasts; different
distribution of body fat

1
Anthropoid body mass from Plavcan and van Schaik (1997b). Strepsirrhine body mass dimorphism from Kappeler (1990). Anthropoid
canine dimorphism from Plavcan and van Schaik (1992). Strepsirrhine canine dimorphism from Kappeler (1991). Information on
pelage and other dimorphisms from Hershkovitz (1977), van Schaik et al. (1999), Crook (1972), and Fleagle (1999).
J.M. Plavcan] DIMORPHISM IN PRIMATES
Fig. 2. Occlusal views of maxillary canine teeth of five pri-
mates, illustrating variation in canine size and shape among
species, and within sexes. All teeth are oriented in same direc-
tion, with mesial at top, distal at bottom, lingual to left, and
buchal to right. Note especially progression from strongly com-
pressed in Varecia to rounded in Pongo, the heart-shaped outline
of male Macaca and Presbytis teeth associated with a deeply
excavated mesial groove, and differences in shape between males
and females of Macaca and Presbytis.
females. Among anthropoids, male canines vary in
size and shape (Fig. 2), ranging from fat, relatively
short teeth in the great apes (by comparison to cer-
copithecoids), to long, tall thin teeth in hylobatids
(Greenfield and Washburn, 1991; Greenfield, 1992a;
Plavcan, 1993a). Dimorphism is usually much
greater in the crown height of the tooth than in the
occlusal dimensions (the measurements of length
and breadth at the base of the tooth). There are
distinctive patterns of canine dimorphism that cor-
respond roughly to differences in male canine shape.
Cercopithecoids tend to show proportionally greater
crown height dimorphism as compared to occlusal
dimorphism, while in hominoids dimorphism tends
to be more uniform among the tooth dimensions.
Male and female canines in many species cannot
be easily sorted when they are similar in size. How-
ever, Kelley (1995a,b) demonstrated that hominoid
male and female canine teeth can be sorted on the
basis of a few simple proportional differences, even
where they do not differ substantially in size. Many
male anthropoid canines are characterized by a
strong mesial groove running down the anterior
29
surface of the tooth onto the root (Crook, 1972;
Fleagle, 1999). This gives the tooth a heart-shaped
occlusal outline which is easily recognized, espe-
cially in cercopithecoids.
While most female anthropoids have smaller ca-
nine teeth than males, their canines nevertheless
can be quite large (Plavcan and van Schaik, 1994;
Plavcan et al., 1995). Female canine tooth size
ranges from small, as in most colobines, to as large
as those of males, as in the hylobatids. Females of
some species also have a mesial groove, though not
as exaggerated as that of males. Importantly, canine
tooth size dimorphism is as much a function of vari-
ation in female canine tooth size as male canine
tooth size. For example, both Callicebus and Hylo-
bates show nearly monomorphic canine teeth. In
Callicebus, canines in both sexes are relatively short
and blunt, while in Hylobates, they are relatively
tall.
The mandibular premolar that lies adjacent to the
mandibular canine (P2 in platyrrhines and P3 in
catarrhines) can also be highly dimorphic (Zingeser,
1969; Crook, 1972; Greenfield, 1992a,b, 1996;
Greenfield and Washburn, 1992). In most species,
the male tooth is elongated to form a hone for
sharpening the back edge of the maxillary canine
tooth (Fig. 3). Consequently, the mandibular premo-
lar is often considered with the canines as part of the
canine/premolar complex. Females also can have
an elongated premolar. Greenfield (1996) offers evi-
dence that the hone of the female mandibular pre-
molar is overdeveloped by comparison to the size of
the maxillary canine. He proposes that the develop-
ment of the female hone is a genetic correlated-
response to the development of the male honing
tooth. However, female canine crown height is
strongly correlated with female honing premolar
length, suggesting that the hone is functional in
females as well as in males (though this does not
rule out the effect of correlated response).
Dental and skeletal dimorphism. Primates also
show sexual dimorphism in the skeleton and teeth.
Linear dimensions of the noncanine teeth can be up
to about 10% larger in males than females (Garn et
al., 1966; Plavcan, 1990; Cochard, 1985). It has been
suggested that there is a field effect of sexual di-
morphism in the dentition, centered on the canine
teeth, such that teeth closer to the canines tend to be
more dimorphic than those farther away (Garn et
al., 1966). Others have suggested that different taxa
share different patterns of sexual dimorphism in the
teeth (Lieberman et al., 1985; Oxnard, 1987). It ap-
pears, however, that noncanine tooth size dimor-
phism is largely a correlate of body mass dimor-
phism (Cochard, 1985; Wood et al., 1991). While the
pattern of tooth size dimorphism in the dentition
tends to follow classic fields of tooth size, there are
no substantial, taxonomically significant patterns of
dimorphism in teeth other than the canines (Plav-
can, unpublished findings).
30 YEARBOOK OF PHYSICAL ANTHROPOLOGY
Fig. 3. Lateral views of mandibular canines and honing pre-
molars of four anthropoid species. A: Pan troglodytes. B: Man-
drillus leucophaeus. C: Alouatta seniculus. D: Macaca mulatta.
Mesial is to left, distal to right. Note strong elongation of the hone
in Macaca and Mandrillus, in both males and females. In Pan,
the mesial enamel face of the tooth is extended, but not clearly
derived as in the cercopithecoids.
Cochard (1985) noted that dimorphism of the mo-
lar and premolar teeth is less than expected on the
basis of body mass dimorphism. He suggested that
males of dimorphic primates tend to have relatively
small teeth for their body size because size dimor-
phism is achieved largely through an extension of
male growth, continuing well after tooth size has
been determined.
Cranial and skeletal dimorphism in primates is
less well-studied than canine or body mass dimor-
phism (Wood, 1976; Anderson, 1981, 1982; Leu-
tenegger and Larson, 1985; Richtsmeier and Chev-
erud, 1989; Corner and Richtsmeier, 1991, 1992,
1993; Ravosa, 1991; Richtsmeier et al., 1993; Ravosa
and Ross, 1994; Lague, 2000). As a rule, skeletal
dimorphism tends to be pronounced in more size-
dimorphic primates: larger males have proportion-
ally larger skeletons (Wood, 1976). Hence, skeletal
dimorphism clearly arises primarily as a conse-
quence of size dimorphism, and not as a consequence
of selection for different male and female adapta-
tions (even though there is good evidence that mor-
phological dimorphism in some other vertebrates
and invertebrates is a direct consequence of niche
[Vol. 44, 2001
Fig. 4. Range of dimorphism of 38 measurements of skull and
jaws in Macaca nemestrina (28 males, 18 females). Dimorphism is
estimated as natural log of the ratio of average male value di-
vided by average female value for each dimension. Measurements
are organized loosely into regions: N, neurocranium; O, orbits; B,
basicranium; P, palate; F, face; M, muscle attachments; J, jaws.
Note that dimorphism is strongest in the palate, face, muscle
attachment surfaces, and jaws, and least in the basicranium,
orbits, and neurocranium. However, there is a substantial range
of variation within these regions.
divergence between males and females; Andersson,
1994). Dimorphism of linear skeletal dimensions
tends to be proportional to the cube root of body
mass dimorphism (Gingerich, 1981). For example, a
species showing a body mass dimorphism ratio of 1.5
(males 50% larger than females) can be expected
show dimorphism of about 1.14 (males 14% larger
than females) in linear skeletal dimensions.
This proportionality between mass and skeletal
dimorphism is only a generalization. Skeletal dimor-
phism is not uniformly expressed as a simple func-
tion of body mass dimorphism in primates (Oxnard,
1987; OHiggins et al., 1990; Wood et al., 1991; Plav-
can, in press), and in fact appears to be very complex
in the pattern of its expression both within and
among species. In most species, measurements of
the brain case, basicranium, and orbits tend to show
less dimorphism than measurements of the face and
jaws (Fig. 4; Leigh and Cheverud, 1991; Ravosa,
1991; Ravosa and Ross, 1994; Corner and Richts-
meier, 1991, 1992, 1993; Masterson, 1997; Master-
son and Hartwig, 1998; Lockwood, 1999; Plavcan, in
press). However, measurements of a single bone,
such as the mandible, can show substantially differ-
ent degrees of dimorphism within and among spe-
cies. For example, in a sample of 80 Gorilla speci-
mens, males are on average 8% larger than females
J.M. Plavcan] DIMORPHISM IN PRIMATES
Fig. 5. Profile of dimorphism in 38 craniofacial dimensions for
three species of Alouatta. Note the general similarity of profiles,
indicating that all three species share similar patterns of cranio-
facial dimorphism. Dimorphism is measured as natural log of the
ratio of average male measurement divided by average female
measurement for each dimension.
in mandibular depth, but 29% larger than females in
mandibular symphyseal thickness. In Colobus ango-
lensis, males are about 14% larger than females in
both dimensions. In fact, there is a hierarchy of
variation in patterns of dimorphism: there is a basic
pattern of dimorphism among skeletal components,
but species vary in patterns that are superimposed
on this general pattern (Plavcan, in press).
Patterns of craniofacial dimorphism tend to be
conserved among closely related species (Plavcan, in
press; but see Jones et al., 2000, for evidence of
variation in craniofacial dimorphism among subspe-
cies of Alouatta paliatta). Thus, species of Alouatta
(Fig. 5) tend to show much more similar patterns of
craniofacial dimorphism to each other, than to, for
example, Macaca (Plavcan, in press). Great apes are
unusual in that, proportional to their body mass
dimorphism, they tend to show less craniofacial di-
morphism than other primates (Plavcan, in press).
This observation is intriguing for those interested in
understanding hominid dimorphism, because it im-
plies that the intense craniofacial dimorphism of
some hominids is associated with even greater body
mass dimorphism than formerly suspected (cf. Lock-
wood, 1999).
In contrast, no such taxonomic patterns are found
in the dentition, apart from those seen in the canine/
premolar complex (Wood, 1976; Wood et al., 1991;
Plavcan, unpublished findings). Lague (2000) re-
cently found little evidence for significant pattern
differences in dimorphism of the elbow and knee
joint surfaces in a series of catarrhine primates.
Likewise, Wood (1976) found little evidence for sub-
stantial pattern differences in the postcranial skel-
31
etons of seven primate species. Beyond this, compar-
ative studies of pattern differences in dimorphism
are relatively few, so it is no surprise that the causes
of such differences are poorly known. The complex-
ity of the results of the above studies suggests a
variety of factors underlying pattern differences in
skeletal and cranial dimorphism.
Some basic pattern differences can be easily ex-
plained. For example, colobine primates show little
body mass dimorphism, but rather intense canine
tooth size dimorphism (Plavcan and van Schaik,
1997b). Consequently, only those craniofacial di-
mensions near the canine teeth show substantial
dimorphism (Plavcan, in press). Conversely, cerco-
pithecine primates all show intense body mass and
canine tooth size dimorphism and intense craniofa-
cial dimorphism (Plavcan and van Schaik, 1997b;
Plavcan, in press). Hence the contrasting patterns of
craniofacial dimorphism of colobines and cerco-
pithecines seem to directly reflect the contrasting
patterns of canine and body mass dimorphism.
More subtle differences in patterns of dimorphism
probably reflect interactions between growth pat-
terns and functional and biomechanical constraints,
though there has been little comparative work on
this topic. Leigh (personal communication) noted
that patterns of sutural closure and epipheseal fu-
sion throughout the skeleton vary among primates.
Such developmental variation is likely to influence
the expression of sexual dimorphism in the skeleton
by varying the relative duration of growth among
skeletal components. Studies of craniofacial devel-
opment generally point to patterns of ontogenetic
scaling between males and females, i.e., male
growth curves tend to be extensions of the female
growth curves (Leutenegger and Masterson,
1989a,b; Richtsmeier and Cheverud, 1989; Master-
son and Leutenegger, 1990; Ravosa, 1991; Corner
and Richtsmeier, 1991, 1992, 1993; Richtsmeier et
al., 1993; Ravosa and Ross, 1994). Heterogeneity in
the rate and duration of growth among different
skeletal regions accounts for different patterns of
dimorphism. For example, in baboons, facial dimen-
sions grow faster than neurocranial dimensions.
With extended male growth, this means that facial
dimensions tend to be more dimorphic than neuro-
cranial dimensions.
Potential biomechanical or functional reasons for
variation in patterns of dimorphism are not well
understood at this time. In the craniofacial complex,
simply supporting large canine teeth requires large
jaws and maxillae. In order to effectively use large
canine teeth, an animal needs to open its jaws wide
enough for the canines to clear the mandibular den-
tition (Lucas et al., 1986; Lucas, 1981). The long
faces of many male papionine primates, and the
attendant facial dimorphism, may reflect selection
to increase gape in order to do this (Lucas, 1981; but
see also Ravosa, 1990). On the other hand, recent
studies found no evidence of shape differences in
humeral and femoral joint surfaces (Lague, 2000) or
32 YEARBOOK OF PHYSICAL ANTHROPOLOGY
the craniofacial complex (Spencer and Hogard,
2001) that might reflect selection for different bio-
mechanical properties. The postcranial data are par-
ticularly interesting in light of the hypothesis of
Stern and Susman (1983) that Australopithecus afa-
rensis males and females may have shown different
locomotor repertoires based on postcranial varia-
tion.
Some pattern differences can be explained with
reference to static adult allometric relations be-
tween skeletal size and muscle and/or organ size.
For example, larger male body mass is usually ac-
companied by more robust skeletal components,
more intense development of muscle scarring, and
stronger cresting of bones in comparison to females.
Such differences are manifest even in humans,
which are only modestly dimorphic in body mass
(males less than 20% larger than females), making it
possible to identify the sex of individuals with be-
tween 80 90% accuracy (White and Folkens, 1991).
It is well known that the large sagittal and nuchal
crests of male gorillas are a function of the dispro-
portionate increase in the size of the temporalis
muscles and nuchal musculature as compared to the
brain. Brain size in male and female gorillas is on
average quite similar, even though male gorillas can
be twice the body mass of females (Smith and
Jungers, 1997; Plavcan and van Schaik, 1997b).
This means that the brain case in males and females
is very similar in size. The larger male body mass,
though, means that the muscles attaching to the
brain case require substantially more attachment
area in males than in females. Consequently, males
develop large crests and flanges to provide this ad-
ditional bony surface area.
In a comparative context, however, the relative
development of sagittal and nuchal cresting in pri-
mates is itself a function of overall body size. Be-
cause muscle force is a function of cross-sectional
muscle area, rather than mass, muscle force in-
creases by the 2/3 power of body mass. This means
that larger primates need proportionally larger
muscles in order to maintain an isometric relation-
ship between body size and muscle force. This in
turn requires proportionally larger muscular attach-
ment areas for larger primates. As a result, smaller
primates tend to have less cresting on the skull than
larger primates, regardless of degree of body mass
dimorphism or brain size.
Finally, one other unusual skeletal dimorphism is
found in male gibbons and howler monkeys, which
possess enlarged, hollow hyoid bones that serve as
resonators for the voice.
Much more research needs to be done to under-
stand the underlying causes of variation in patterns
of skeletal dimorphism in primates. Such research is
likely to increase our understanding not only of the
causes of skeletal dimorphism, but also of the
growth, development, constraints, and adaptations
of the skeleton. Skeletal dimorphism often repre-
sents a significant degree of morphological variation
[Vol. 44, 2001
within a species that needs to be accommodated
within any model of the evolution of morphological
form.
Pelage and skin dimorphism. Pelage and skin
can be strikingly dimorphic in primates. The most
familiar example is the brightly colored face of male
mandrills as compared to that of females (Setchell
and Dixson, 2001). Skin and pelage differences are
not limited to mandrills. As already noted above,
there are dramatic female estrous swellings in many
anthropoid species. Proboscis monkeys get their
name from the enormous, pendulous nose of the
male. Guenons are famous for the red-white-and-
blue display of males. The male penis is bright red,
the scrotum is bright blue, and the genital region is
surrounded by white fur. This makes for a conspic-
uous penile display that is used as a threat gesture
by males (Fedigan and Fedigan, 1988). Male gelada
baboons are characterized by a large mane which
probably serves to make males appear larger (Crook,
1972), and might serve as a signal to females of male
health. Orangutan males possess large cheek
flanges and laryngeal pouches. In several species
(Lemur macaco, Pithecia pithecia, Alouatta caraya,
Hylobates concolor, H. hoolock, and H. pileatus),
males and females differ dramatically in pelage
color (Crook, 1972; Hershkovitz, 1977). A number of
other species show minor sex differences in pelage
color or patterning (Hershkovitz, 1977; Napier,
1981, 1985). The reasons for this are not clear,
though it could be related to mate recognition (as a
function of speciation), mating preferences, or fe-
male choice (Crook, 1972; Hershkovitz, 1977; Martin
et al., 1994).
CAUSAL MODELS
Sexual selection
Sexual dimorphism in body mass, canine tooth
size, and display features is commonly attributed to
sexual selection. However, there are other factors
including developmental, phylogenetic, and genetic
constraints, natural selection, and epiphenomenal
factors that can influence the expression of dimor-
phism in species (Crook, 1972; Clutton-Brock et al.,
1977; Leutenegger and Kelly, 1977; Harvey et al.,
1978; Leutenegger and Cheverud, 1982, 1985; Gau-
lin and Sailer, 1984; Cheverud et al., 1985; Clutton-
Brock, 1985; Gautier-Hion and Gautier, 1985; Leu-
tenegger and Lubach, 1987; Shea, 1986; Oxnard,
1987; Kay et al., 1988; Ely and Kurland, 1989; Kap-
peler, 1990, 1991, 1996; Greenfield, 1992a,b, 1996;
Leigh, 1992, 1995a,b; Plavcan and van Schaik, 1992,
1994, 1997b; Ford, 1994; Martin et al., 1994; Hayes
et al., 1995; Leigh and Shea, 1995; Mitani et al.,
1996; Plavcan, 1998, 1999). The relative importance
of these factors to the expression of dimorphism
among primates has been at times a topic of heated
debate. In order to reconcile the sometimes confus-
ing literature on this topic, a review of mechanisms
J.M. Plavcan] DIMORPHISM IN PRIMATES
of sexual selection, and how they have been quanti-
fied in studies of dimorphism, should help.
Following is a brief, simplified description of mate
choice and mate competition. There is substantial
variation on the themes outlined below. The litera-
ture on primates alone describing different male and
female mating strategies is enormous. The most
comprehensive general review of sexual selection to
date is that of Andersson (1994).
Sexual selection encompasses a diverse array of
mechanisms (Andersson, 1994). Sexual selection
theory is broadly divided into two components: mate
competition and mate choice. Individuals can in-
crease their reproductive fitness relative to conspe-
cific rivals by either excluding rivals from mating
(mate competition), or by selectively choosing mates
(mate choice). Both of these mechanisms generate
selection by increasing the fitness of offspring (if
mates who win fights or are chosen pass on better
genes), and/or by creating differential mating oppor-
tunities (by excluding some individuals from mat-
ing, either by force or by active choice). Neither
mechanism is limited to one or the other sex. How-
ever, in primates mate competition is largely asso-
ciated with males, while mate choice is associated
with females.
Mate choice and mate competition theoretically
arise ultimately from anisogamy (differential size
and production of gametes between sexes), which in
turn favors different levels of parental investment in
individual offspring (Trivers, 1972; Reynolds and
Harvey, 1994; Andersson, 1994). In primates, males
are limited in their reproductive output by the num-
ber of females that they can inseminate. Sperm sup-
ply for a male can be temporarily reduced through
repeated ejaculation (Dixson, 1997), but the sperm
count rebounds much more quickly than the supply
of females that a male can effectively mate with over
a period of time (cf. van Schaik et al., 1999). Conse-
quently a male can dramatically increase his fitness
relative to other males by excluding them from ac-
cess to a group of females. This provides a powerful
incentive for males to compete intensely with one
another for access to females (Pagel, 1994). Any
weaponry or other morphological feature such as
size, displays, agility, speed, coordination, or other
behaviors that help males win fights should be pow-
erfully selected for (Crook, 1972; Clutton-Brock,
1985; Kappeler, 1991; Martin et al., 1994; Reynolds
and Harvey, 1994; Plavcan, 1999).
The other half of the equation is mate choice.
Generally speaking, a females reproductive output
is limited by the number of offspring she can pro-
duce and raise (Andersson, 1994; Reynolds and Har-
vey, 1994). While a females egg production theoret-
ically can be very large, the costs of pregnancy,
lactation, and child care can be quite high, limiting
the number of offspring that can be produced in a
lifetime. Presumably, the survivorship and repro-
ductive success of the females offspring will be at
least partly a function of the quality of the genes
33
contributed by the male. Male parental investment
also can improve offspring survival (Andersson,
1994; Reynolds and Harvey, 1994). The result is
selective pressure for females to choose their
mates, either to control genetic quality, or to select
for males that will in some way be better providers.
Female choice is not necessarily limited to char-
acters that signal male fitness. For example, if fe-
males have, for some reason, a preexisting bias to
mate with males bearing a particular trait, then
selection might favor the development of that trait,
even if it is not associated with any fitness benefit
(Fisher, 1930; Ryan, 1990; Andersson, 1994; Stall-
mann and Froehlich, 2000). Another mechanism
that may produce dimorphism is mate recognition.
Females or males may prefer traits that act as sig-
nals to ensure conspecificity, avoiding cross-breed-
ing with closely related species that may produce
less viable offspring. While these mechanisms are
known among biologists interested in sexual selec-
tion (Andersson, 1994), they have not received a
great deal of scrutiny among primatologists inter-
ested in dimorphism.
History of comparative studies of dimor-
phismsexual selection vs. other mechanisms.
The hypothesis that sexual dimorphism in primates
is a consequence of mate competition has had a long
historical development, during which various alter-
native explanations for the evolution of dimorphism
were put forward. The way that mate competition is
measured and analyzed, and views on its relative
importance in explaining the evolution of dimor-
phism in primates, are intertwined with the devel-
opment of these alternative hypotheses. Hence, be-
fore presenting a detailed review of recent
comparative studies of the sexual selection hypoth-
esis and dimorphism in primates, it will be helpful to
review comparative studies of dimorphism over the
past 30 years. Following this, I shall present a de-
tailed review of recent models of mate competition,
mate choice, and dimorphism. This is followed by a
more detailed discussion of evolutionary models for
other behavioral, ecological, and morphological cor-
relates of dimorphism.
Mate competition has long been thought to be the
primary mechanism favoring the development of
sexual dimorphism in primates (Darwin, 1871;
Crook, 1972; Leutenegger and Kelly, 1977; Clutton-
Brock, 1985; Kay et al., 1988; Kappeler, 1990, 1991;
Plavcan and van Schaik, 1992, 1994, 1997b; Ford,
1994; Martin et al., 1994; Lindenfors and Tullberg,
1998). In easily observed species, such as baboons,
males are largely intolerant of one another, often
engaging in spectacular fights and threat displays.
Such displays and fighting seem to determine access
to females. Species like baboons are intensely dimor-
phic. Males have enormous canine teeth and are
much larger than females, fitting well with the con-
cept that sexual selection has favored these traits
because of the advantages they confer in winning
34 YEARBOOK OF PHYSICAL ANTHROPOLOGY
fights. In contrast, monomorphic gibbons are very
obviously monogamous, showing no apparent differ-
ential male reproductive success that is associated
with male-male competition.
Sexual selection is not the only explanation for
sexual dimorphism in primates. One of the oldest
alternative hypotheses is that large male body size
and canine tooth size evolved for predation defense
(DeVore and Washburn, 1963). In fact, the popular-
ity of the sexual selection hypothesis as an explana-
tion for the evolution of primate sexual dimorphism
has actually waxed and waned over the years. This
has come about partly as a result of the failure of
many studies to adequately demonstrate a relation
between variation in dimorphism and variation in
estimates of sexual selection, and partly through the
elaboration of alternative mechanisms that might
explain variation in dimorphism.
Debates in the comparative literature of the past
30 years were stoked by the observation that sexual
dimorphism in body mass and canine tooth size var-
ies considerably in magnitude across primates
(Clutton-Brock et al., 1977; Leutenegger and Kelly,
1977; Harvey et al., 1978; Pickford, 1986; Martin et
al., 1994; Plavcan and van Schaik, 1994). At the
same time, as more became known about primate
social systems, behavior, and ecology, it became ap-
parent that sexual selection must vary in intensity
among species. This led to attempts to associate
variation in sexual dimorphism with variation in
estimates of sexual selection. The first such at-
tempts were anecdotal. Crook (1972) observed the
association between polygyny and dimorphism in
primates, and provided detailed hypotheses for the
evolution of dimorphism in pelage, body size, canine
size, and other morphological traits in relation to
various mating systems and habitats. Leutenegger
and Kelly (1977) presented a comparison of dimor-
phism in canine size and body mass in primates.
They concluded that dimorphism in the two charac-
ters is moderately correlated, suggesting that fac-
tors other than sexual selection may play a role in
constraining or driving the evolution of dimorphism
in different characters in different species. For ex-
ample, in addition to sexual selection, they sug-
gested that predation defense may play a role in the
evolution of large body size in male proboscis mon-
keys, but that an arboreal mode of locomotion may
constrain the evolution of large male size in other
colobines, thereby constraining the expression of
body mass dimorphism.
Clutton-Brock et al. (1977) attempted the first
formal statistical test of the sexual selection hypoth-
esis in primates. They measured sexual selection
using the socionomic sex ratiothe number of adult
females in a typical group divided by the number of
adult males. The reasoning behind this ratio is that
the fewer males per group, the greater the differen-
tial male reproductive success associated with male-
male competition. Hence, the greater the ratio, the
more intense sexual selection must be. They found a
[Vol. 44, 2001
weak positive correlation between the socionomic
sex ratio and body mass dimorphism. However, they
noted that when monogamous species were removed
from the analysis, there was no correlation between
the socionomic sex ratio and dimorphism, even
though there is a large range of variation in both
variables. They noted that this could reflect either
the effect of other factors on the evolution and ex-
pression of sexual dimorphism, or the inadequacy of
the socionomic sex ratio to capture variation in sex-
ual selection (now widely accepted; cf. Clutton-
Brock, 1985; Andersson, 1994; Plavcan, 1999). They
also noted that terrestrial species tend to be more
dimorphic than arboreal species, and that body mass
dimorphism is significantly positively correlated
with overall body size. They suggested that the dis-
tinction between terrestrial and arboreal species
might reflect a constraint on larger male size asso-
ciated with the use of terminal branches in arboreal
species.
Harvey et al. (1978) provided the first statistical
comparative analysis of canine tooth size dimor-
phism. To estimate sexual selection, they used a
tripartite categorization of primate mating systems:
monogamy, multimale/multifemale social groups,
and single-male/multifemale harems. They rea-
soned that sexual dimorphism should be minimal in
monogamous primates because there is little male
differential reproductive success. Dimorphism
should be intermediate in multi-male groups, and
greatest in single-male groups, reflecting the ability
of males to either partially or totally exclude other
males from access to a group of females. They found
that monogamous species are indeed less dimorphic
than polygynous species, but they found no signifi-
cant difference in dimorphism between the multi-
male and single-male social systems. They too noted
that terrestrial species are more dimorphic than
arboreal species, supporting the predation-defense
hypothesis.
Up to this point, studies confirmed that sexual
selection has something to do with the evolution of
sexual dimorphism in primates, but they also sug-
gested that much of the variation in dimorphism
among species must reflect other factors. Subse-
quently, two influential studies suggested that the
evolution of larger body size alone leads to the evo-
lution of greater sexual dimorphism (Leutenegger
and Cheverud, 1982, 1985), and that phylogenetic
inertia explains a great deal of variation in dimor-
phism (Cheverud et al., 1985).
Leutenegger and Cheverud (1982, 1985) devel-
oped a quantitative genetic model which suggested
that sexual dimorphism will increase over time if
male traits are more variable than those of females,
or if male traits are less heritable. This hypothesis
was put forward to explain the well-known correla-
tion between sexual dimorphism and body mass in
primates (Crook, 1972; Clutton-Brock et al., 1977;
Harvey et al., 1978; Pickford, 1986; Plavcan and van
Schaik, 1992, 1994, 1997b; Plavcan, 1999). However,
J.M. Plavcan] DIMORPHISM IN PRIMATES
it also suggested that sexual selection may play a
relatively minor role in the evolution of sexual di-
morphism.
The analysis received a variety of intense criti-
cism. Gaulin and Sailer (1984) pointed out that the
measure of sexual dimorphism used in the study
was biologically unrealistic, de facto creating a
strong correlation between size and dimorphism.
Leutenegger and Cheverud (1982, 1985) treated a
5-kg difference in mass the same between galagoes
and gorillas. For a galago to show proportionally as
much dimorphism as a gorilla by this measure, the
male galago would have to weigh over 1,000 times as
much as the female. Plavcan and Kay (1988) and
Plavcan (1990, 2000b) demonstrated that male pri-
mates are not relatively more variable than females
for dental and cranial traits. Kappeler (1990, 1991)
and Godfrey et al. (1993) pointed out that there is no
correlation between body size and dimorphism in
strepsirrhine primates. Andersson (1994) noted that
several studies likewise found little such correlation
in other groups of animals, and that the model only
works as long as body size continually increases in a
lineage over time. It is interesting to note that in the
human lineage, dimorphism apparently has de-
creased through time while body size has increased
(Frayer, 1980; McHenry, 1992).
In spite of all this criticism, it is important to
emphasize that the model of Leutenegger and Chev-
erud (1982, 1985) has not been disproved. The above
criticisms primarily targeted the analysis of Leu-
tenegger and Cheverud (1982, 1985), but not the
model itself, which incorporates selective and non-
selective components, and is based on established
quantitative genetic work by Lande (1980). All of the
above papers have critiqued only the suggestion that
body size increase is the primary factor driving the
evolution of dimorphism in primates, by critiquing
the claims of a strong correlation between body size
and dimorphism, and greater male character varia-
tion. The critiques of the correlation between size
and dimorphism do not deny the widely acknowl-
edged fact that such a correlation exists in anthro-
poid primatesthey only point out that Leuteneg-
ger and Cheverud (1982, 1985) overemphasized the
correlation through the way that they measured
dimorphism, and that such a correlation does not
exist in other groups of mammals. Even arguments
about male and female trait variability are not con-
clusive. Plavcan and Kay (1988) and Plavcan (1990,
2000b) demonstrated that male traits are not rela-
tively more variable than female traits. But in terms
of absolute variation, there is little doubt that male
primates tend to be more variable than females. The
key is deciding which is more important: relative or
absolute variation. Given that absolute variation is
fundamentally linked to size itself, this particular
question about male and female variability is diffi-
cult to resolve.
In another important paper, Cheverud et al.
(1985) suggested that much variation in dimorphism
35
among primates can be explained as a correlate of
taxonomy, and not sexual selection. They used an
autocorrelation model to partition variation in di-
morphism correlated with taxonomy from that
which is correlated with body size, mating system,
habitat, and diet, and found that taxonomy explains
50% of the variation, body size explains 36%, and
habitat, mating system, and diet explain the rest.
Ely and Kurland (1989) reanalyzed the data of
Cheverud et al. (1985), and challenged their conclu-
sions. Regardless of the validity of the model or the
interpretation of the results, Cheverud et al. (1985)
brought the concept of phylogenetic inertia to the
forefront of analyses of sexual dimorphism. While
taxonomic differences in dimorphism have been
known for a long time (cf. Crook, 1972), they had
been largely ignored as a potential explanatory or
confounding factor in understanding dimorphism
among primates. Almost all comparative analyses of
dimorphism in primates now acknowledge the exis-
tence of taxonomic correlations, and the potential
importance of phylogenetic inertia as an explanation
for variation in the magnitude and expression of
dimorphism among species.
Other hypotheses received support in various pa-
pers over the years. Rowell and Chism (1986) pre-
sented evidence of multimale influxes and matings
in supposedly single-male species of guenons. They
suggested that the role of sexual selection and male-
male competition had been overemphasized. Phil-
lips-Conroy and Jolly (1981) likewise questioned the
role of sexual selection, noting that the magnitude of
dimorphism in hamadryas and olive baboons did not
appear to follow the pattern predicted by mating
systems. A number of papers emphasized the role
that predation defense must play in the evolution of
sexual dimorphism (Crook, 1972; Leutenegger and
Kelly, 1977; Gautier-Hion and Gautier, 1985; Rowell
and Chism, 1986; Plavcan and van Schaik, 1992,
1997b), based on the observation that terrestrial
species tend to be more dimorphic than arboreal
species. Leutenegger and Lubach (1987) pointed out
that Cercopithecus neglectus is apparently monoga-
mous, yet is among the most dimorphic of guenons.
They suggested that dimorphism is retained in this
species as a consequence of phylogenetic inertia.
Several papers entertained the concept of niche di-
vergence in primates (e.g., Clutton-Brock et al.,
1977; Harvey et al., 1978), though none has ever
provided compelling field data for this hypothesis.
Some suggested that arboreal locomotion places an
upper limit on male body size, constraining the ex-
pression of body size dimorphism (Clutton-Brock et
al., 1977; Leutenegger and Kelly, 1977). Lucas
(1981) suggested that maximum jaw gape may con-
strain male canine crown height, constraining ca-
nine dimorphism. He also suggested that enlarged
male canines evolved in an anthropoid ancestor, and
that variation in canine dimorphism is a function of
gape constraints.
36 YEARBOOK OF PHYSICAL ANTHROPOLOGY
TABLE 2. Major factors thought to affect body mass dimorphism and canine dimorphism in primates
Factor Effect
Male-male competition Increased male size, weaponry,
display
Predation Increased male size, weaponry
Body size
a) Lower limit on body size favoring No dimorphism in small,
speed or agility over absolute size polygynous species
differences
b) Lower male trait heritability, Male trait size increases faster
increased male trait variance than females with increasing
body size
c) Larger female groups at larger Increased male competition, size,
size weaponry
Substrate
a) Arboreality Upper limit on male size, limiting
dimorphism
b) Larger female group size leading Increased male size, weaponry,
to male-male competition display
c) Females easier to guard/coerce Increased male size, weaponry,
display
Phylogeny Inherited patterns of behavior,
ecology, or morphology limit
variation in dimorphism within
taxonomic groups
Niche Dimorphism Separation of male and female
ecological niches favors different
morphologies
Female competition Increased female size and
weaponry reduce dimorphism
Timing of female maturation Selection for early or delayed
maturation may increase or
decrease female size
Diet
a) Less energy for folivores Constraint on male size, or male
competition in folivores
b) Minimum body size in small Selection to slow gut-passage time
arboreal species favors large females, reduces
dimorphism
c) High female energetic Favors smaller female body size,
requirements from pregnancy, increased size dimorphism
lactation
d) Reduction of canines for dietary Reduction in canine dimorphism
use following relaxed sexual selection
e) Dietary specialization Reduced canine dimorphism if
canines used for seed predation
in both sexes
Gape Male canine size limited by
maximum jaw opening
Correlated response Common genetic control constrains
independent expression of male/
female traits
Display Increased display, exaggerated
weaponry
1
See text for references and detailed descriptions.
2
OSR, operational sex ratio.
[Vol. 44, 2001
Evidence1
Correlation of canine/mass dimorphism
with competition levels, mating
system, OSR2
Terrestrial species more dimorphic
than arboreal
Polygynous Malagasy lemurs show no
dimorphism
Dimorphism correlated with size; male
characters not relatively more
variable than females
OSR, competition levels, female group
size increase with increasing size
Arboreal species less dimorphic than
terrestrial
OSR, competition levels, female group
size larger in terrestrial species
Speculative
Dimorphism, behavior, and ecology
covary with phylogeny
Little evidence
Female canine size covaries with
female agonistic competition
Relative timing of female maturation
correlated with diet/social system
Weak evidence that folivores are less
dimorphic
Smaller folivores are less dimorphic
Theoretical
Contact between maxillary lateral
incisor and mandibular canine
enhanced in small canines
Clearly specialized canines in
pithecines
Correlation between canine crown
height and mandibular dimensions
Correlation between relative male and
female canine size in absence of
female agonistic competition
Increased canine dimorphism, display
features in multimale societies:
canine dimorphism correlated with
competition levels, but not OSR

At the very least, the results of all of these studies
have led to a general recognition that dimorphism is
multifactorial in expression and cause, following the
suggestion of Oxnard (1987). While there is little
doubt now that sexual dimorphism is not a single
character, and that there are multiple factors that
affect its evolution and expression (Table 2), it has
not been clear which factors are most important in
the evolution of dimorphism, and which play second-
ary roles. Several papers expressed the opinion that
sexual selection plays a minor, if any, role in ex-
plaining variation in dimorphism among living pri-
mate species (Lucas, 1981; Phillips-Conroy and
Jolly, 1981; Rowell and Chism, 1986).
Recent models of mate competition, intrasexual
competition, and dimorphism. A series of pa-
pers since the late 1980s reevaluated the sexual
J.M. Plavcan] DIMORPHISM IN PRIMATES
selection hypothesis, focusing on the problem of how
to measure sexual selection. Early studies acknowl-
edged the potential shortcomings of mating system
and socionomic sex ratio as measures of sexual se-
lection (Clutton-Brock et al., 1977; Harvey et al.,
1978). To measure sexual selection, one should ide-
ally obtain accurate data on male reproductive suc-
cess over time, coupled with information on male
intrasexual competition that directly leads to such
differential reproductive success. To test the hypoth-
esis that any particular character evolves as a con-
sequence of sexual selection, one needs data on
whether the character actually plays a role in the
outcome of competitive bouts that result in differen-
tial male reproductive success, and whether the
morphology of the character follows a predicted di-
rection. In short, one needs to show that bigger
males with bigger canines win more fights against
other males, and as a result that they sire more
offspring. Such data are not available for the over-
whelming majority of species. Hence, all tests of the
sexual selection hypothesis use surrogate measures
of sexual selection that are derived from behavioral
and demographic data that are assumed to reflect
the strength of sexual selection (Mitani et al., 1996;
Plavcan, 1999). This issue is critical in any attempt
to claim that one factor is more or less important
than another in the evolution of sexual dimorphism.
How can we assert that body size is more important
than sexual selection in the evolution of dimorphism
if our measure of sexual selection does not measure
sexual selection?
Kay et al. (1988) attempted to directly estimate
the magnitude of male-male competition in platyr-
rhine primates. They ranked each species into a
competition level. The lowest level contained spe-
cies where males were not seen to compete much at
all. The highest level contained species in which
male-male competition occurred in the context of
year-round agonistic dominance hierarchies. Kay et
al. (1988) found a strong relationship between com-
petition levels and canine dimorphism.
Plavcan and van Schaik (1992) formalized the
competition level system, and applied it to all an-
thropoids. They used dichotomous estimates of the
intensity and potential frequency of male-male com-
petition. Intensity was defined as whether males are
tolerant or intolerant of one another. Potential fre-
quency was basically a dichotomous demographic
measure of whether one, or more than one, male
typically occurred with a group of adult females. If
more than one adult male occurred in a group, ago-
nistic competition could potentially happen on a
daily basis. The low-frequency class also contained
species in which males were normally tolerant, ex-
cept during a limited breeding season, as well as
species typified by single-male harems with multi-
male influxes during a limited breeding season. In-
tensity and potential frequency classifications were
combined into four competition levels. Dimorphism
in both canine tooth size (Plavcan and van Schaik,
37
1992) and body mass (Plavcan and van Schaik,
1997b) were significantly associated with compe-
tition levels, and with the separate intensity and
frequency classifications. More importantly, the
relationship between competition levels and di-
morphism held within dietary categories, within
substrate classifications, and within a variety of
taxonomic groups. This strongly suggested that
sexual selection plays an important role in the
evolution of sexual dimorphism, regardless of the
effect of any other factor.
Close examination of competition levels helps to
explain the poor correlation between mating system
classifications and dimorphism found in earlier
studies (cf. Harvey et al., 1978; Leutenegger and
Cheverud, 1982, 1985; Cheverud et al., 1985; Phil-
lips-Conroy and Jolly, 1981; Rowell and Chism,
1986). Competition levels 2 4 all contain multimale/
multifemale species, but they make distinctions be-
tween the quality of male-male competition among
different multimale breeding systems. For example,
chimpanzee males (competition level 2) are known
to show some agonistic competition, but in general
males are characterized by tolerant relationships
with one another. By contrast, Saimiri males (com-
petition level 3) live together in multimale groups
year round, but only form agonistic dominance hier-
archies during the breeding season. Theropithecus
males (competition level 4) form single-male har-
ems, but these aggregate daily into large groups
where males come into close proximity with one
another.
Competition levels also reversed the predicted di-
rection of dimorphism for the comparison between
single-male and multimale mating systems.
Whereas Harvey et al. (1978) originally suggested
that single-male groups should show the greatest
degree of dimorphism based on differential male
reproductive success, competition levels predicted
that multimale groups with agonistic dominance hi-
erarchies should show the greatest degree of dimor-
phism based on high-frequency, high-intensity com-
petition.
Competition level 1 species are all monogamous or
polyandrous. Plavcan and van Schaik (1992, 1997b)
noted that such species are not necessarily charac-
terized by an absence of male-male competition. For
example, male hylobatids are known to be relatively
intolerant of one another, but engage in low-fre-
quency competition. Technically, they should be
placed in competition level 3. However, because hy-
lobatids form pair-bonds, and females help to defend
territories (hence technically also showing high-in-
tensity, low-frequency competition), dimorphism is
not expected to evolve in hylobatids as a conse-
quence of male-male competition. In a separate
analysis of relative male canine size (not canine
dimorphism), Plavcan (1993a) demonstrated that
hylobatid male canine size is consistent with other
competition level 3 anthropoids.
38 YEARBOOK OF PHYSICAL ANTHROPOLOGY
Plavcan et al. (1995) noted that, like males, female
primates compete agonistically. Consequently, if ag-
onistic competition generates selection to develop or
maintain big canine teeth in male primates, then it
should do so in females too, as long as there is a
fitness consequence to winning and losing fights.
Plavcan et al. (1995) classified male and female an-
thropoids separately by intensity and potential fre-
quency, generalizing the definitions above to apply
to males and females. However, they also noted that
many female anthropoid primates (and males of a
few species) compete agonistically in the context of
coalitions. That is, the outcome of fights is not de-
termined by individuals, but by groups of individu-
als that support each other. In this case, Plavcan et
al. (1995) reasoned that weaponry should not play as
prominent a role in determining the outcome of
fights, and hence that animals that regularly com-
pete in coalitions should have smaller canine teeth
than those that compete in high-intensity, high-fre-
quency dyadic contexts. Plavcan et al. (1995) found a
significant effect of frequency, intensity, and coali-
tionary competition in both male and female anthro-
poids. The analysis was the first to demonstrate a
link between female agonistic behavior and female
canine size. Clearly, canine dimorphism is a func-
tion of selection on both male and female characters.
Another important paper came in the application
of a concept known as the operational sex ratio
(OSR). The theory was laid out by Emlen and Orling
(1977), but not applied to primates until 1996 (Mi-
tani et al., 1996). Emlen and Orling (1977) noted
that differential male reproductive success should
be a function not only of the sex ratio in a popula-
tion, but also of the actual ability of males to mo-
nopolize access to females. In primates, this should
be a function of when females become receptive and
fertile relative to one another. Hence, if female es-
trus and ovulation do not overlap in timing, a single
male can successfully guard each female in a group,
one at a time, preventing the other males from
breeding. However, if females come into estrus and
ovulate simultaneously, a male can only guard one
female at a time, meaning that other males will be
able to successfully mate and reproduce. Mitani et
al. (1996) applied this concept to a sample of 18
polygynous anthropoid primates, and found a signif-
icant association between the operational sex ratio
and body mass dimorphism. This strongly suggests
that previous analyses failed to corroborate the sex-
ual selection hypothesis using mating systems, be-
cause mating systems do not capture variation in
sexual selection. The result also reinforces the im-
portance of focusing on differential male reproduc-
tive success associated with male-male competition
in the evolution of sexual dimorphism.
Interestingly, the OSR is not correlated with ca-
nine tooth size dimorphism. The reasons for this are
not clear. Plavcan (1999) suggests that it might be a
function of either small comparative sample sizes, or
a different selective mechanism operating on canine
[Vol. 44, 2001
tooth size dimorphism. Plavcan (1999) suggests that
competition levels, which are strongly associated
with canine dimorphism, may measure the utility of
canine teeth both as weapons, and as display items.
It may be that high-frequency competition (which
may or may not be associated with a higher or lower
OSR) favors the enhanced development of weaponry
for display. This follows from the idea that physical
competition is potentially dangerous, even to the
winner of a fight. Hence, in the high-frequency,
high-intensity classification, selection may favor
larger canines in order to reduce the actual fre-
quency of physical contact, by allowing the resolu-
tion of conflicts through display rather than fighting.
This idea is not new (e.g., Crook, 1972; Leutenegger
and Kelly, 1977; Harvey et al., 1978), and the result
is consistent with the observed modest correlation
between canine dimorphism and body mass dimor-
phism (Leutenegger and Kelly, 1977; Plavcan and
van Schaik, 1997b).
Taken together, comparisons of competition lev-
els, competition classifications, and the OSR present
a clearer picture of the relationships between sexual
selection, social systems, and sexual dimorphism.
On the one hand, it seems that sexual selection is
indeed an important factor in the evolution of body
size and canine tooth size dimorphism. On the other
hand, sexual dimorphism is clearly a function of
variation in both male and female traits. For exam-
ple, while canine tooth size in both sexes may vary
as a function of male and female agonistic competi-
tion, such competition may be over mates or re-
sources, and the weaponry may be selected for either
its effectiveness in physical combat, or display in
preventing combat. This strongly implies that the
evolution of dimorphism is not truly a function of
differential male reproductive success; rather, it is a
function of differential selection for the development
of male and female traits (Leigh, 1992, 1995a,b;
Martin et al., 1994; Plavcan et al., 1995). In this
sense, sexual dimorphism can be thought of as re-
flecting the fact that male and female traits are
influenced by different functional and selective re-
gimes, which may vary substantially among species
that are classified as superficially sharing similar
mating systems. This may seem obvious, but for
many years the evolution of sexual dimorphism in
primates was seen as a function of sexual selection
acting on male traits, with the female serving as a
baseline of comparison only.
Sperm competition. One other form of male-male
competition has received a great deal of attention in
recent years; sperm competition (Harcourt and
Gardiner, 1994; Harcourt, 1995; Dixson, 1997). Ag-
onistic male-male competition occurs before copula-
tion. However, if a female is inseminated by several
males, then the male producing the most sperm has
the greatest chance of producing offspring. The
chances of fertilizing an egg might also increase if a
male produces sperm that are faster or more capable
J.M. Plavcan] DIMORPHISM IN PRIMATES
TABLE 3. Mechanisms of mate choice that potentially may influence dimorphism in primates
Mechanism
Females favor male trait that signals male fitness or
quality
Females incite male-male competition to mate with
strongest, healthiest males
Females prefer males that can defend against
infanticidal males
Females confuse paternity by mating with multiple
males to defend against infanticide
Female reduction of group size to reduce likelihood
of takeover by infanticidal male
1
See text for detailed discussion and references.
histochemically of fertilizing an egg. While these
latter mechanisms may play some role, there is over-
whelming evidence that testicular volume, density
of seminiferous tubules, and seminal vesicle size are
greater in species with multimale mating systems,
where females mate with more than one male (Har-
court and Gardiner, 1994; Harcourt, 1995; Dixson,
1997). Species such as Brachyteles and Pan are no-
torious in that male-male agonistic competition is
not intense, mating is promiscuous, and testicular
volume is relatively enormous. In fact, testicular
volume is relatively larger in most multimale spe-
cies showing polyandrous mating. Conversely, mo-
nogamous species, and those characterized by sin-
gle-male groups, show relatively small testicular
volume.
Sperm competition illustrates that sexual selec-
tion in primates is not simply a function of whether
males fight for females or not. Males and females
both have reproductive strategies which often con-
flict, leading to the evolution of strategies and coun-
terstrategies. Sperm competition reflects just such a
process. Absent the opportunity to overtly or com-
pletely exclude one another from access to females in
the first place, males pursue competition within the
female reproductive tract.
Mate choice. The role of mate choice in the evo-
lution of sexual dimorphism in primates has re-
ceived less attention than mate competition. Recent
years have seen an increase in the literature dis-
cussing female mating strategies (e.g., Small, 1989;
Smuts and Smuts, 1993; Nunn, 1999; van Schaik et
al., 1999; Stallmann and Froehlich, 2000). These
involve explicit female choice, as well as various
female strategies to counter male mating coercion
and domination (Smuts and Smuts, 1993). There
has been no quantitative comparative analysis of
how female choice and female mating strategies
might affect the expression of sexual dimorphism in
any character, apart from estrous swellings in ca-
tarrhines (Pagel, 1994; Nunn, 1999; Stallmann and
Froehlich, 2000). This probably reflects the fact that
mate choice is difficult to quantify. Nevertheless,
39
1
Effect
Exaggerated male pelage, color, size
Larger male size, weaponry; exaggerated female
displays favored by males
Larger male size, weaponry
Reduced male size, weaponry through tempering
of differential male reproductive success; female
displays that conceal ovulation, but attract
males
Reduced male size, weaponry through tempering
of differential male reproductive success;
increased female weaponry reduces canine
dimorphism
there is anecdotal evidence for the important role
that mate choice may play in the evolution of dimor-
phism.
Female mate choice can take several different
forms among primates (Table 3). In the classic model
of mate choice, females express a preference for
males bearing a certain trait which presumably sig-
nals greater male quality. The trait can be morpho-
logical, as in the bright plumage of many birds, or it
can be behavioral, as in the nest-building activities
of the bower bird. For example, antler development
in white-tailed deer is correlated with male health
(Ditchkoff et al., 2001). Crook (1972) speculated that
the large mane of male Theropithecus serves to en-
hance the apparent body size dimorphism of this
species, a tactic that may be favored in an environ-
ment scarce in resources. However, body size dimor-
phism in Theropithecus is similar to that seen in
other papionines, suggesting that this might not be
the case. Female Theropithecus play an active role in
selecting a mate (Stammbach, 1987), so it would not
seem unreasonable to speculate that females select
male consorts on the basis of pelage condition, which
in turn might reflect male health.
Females may also incite male-male competition in
order to choose the winner of a fight. For example,
Pagel (1994) speculated that female estrous swell-
ings in catarrhines evolved as a result of female-
female competition, inciting the most fit males to
invest heavily in competition for females with the
most exaggerated swelling. Though this hypothesis
receives little comparative support (Nunn, 1999;
Stallmann and Froehlich, 2000), there is clear evi-
dence that female macaques and baboons prefer to
mate with dominant males (Kappeler, 1999; Nunn,
1999; van Schaik et al., 1999).
Recent years have seen growing evidence of the
critical role that infanticide plays in shaping male/
female interactions. Smuts and Smuts (1993) point
out that males should attempt to monopolize access
to females in any way possible, including physical
coercion. The most extreme form of coercion is in-
fanticide, in which the male kills a females offspring
40 YEARBOOK OF PHYSICAL ANTHROPOLOGY
in order to bring about estrus. Given that females
are limited in the number of offspring they can pro-
duce, there should be powerful incentives for fe-
males to develop counterstrategies against infanti-
cide.
Two ways of defending against infanticide should
affect the evolution of dimorphism in primates: a
female can either confuse paternity so that a male
cannot be certain that he is killing his own offspring,
or a female can associate with a male who will pro-
tect her from other infanticidal males.
It is widely hypothesized that females in multi-
male groups mate polyandrously in order to confuse
paternity (e.g., Small, 1989; Smuts and Smuts,
1993; Pagel, 1994; Nunn, 1999; van Schaik et al.,
1999; Stallmann and Froehlich, 2000). Females in
single-male groups are known to seek out sneak
matings with extragroup males. This is thought to
guard against infanticide in the event of a male
takeover (most infanticide in single-male groups oc-
curs immediately after a male takeover). In multi-
male groups, recently immigrated males are most
likely to commit infanticide. Consistent with this is
that females actively seek out matings with recent
immigrant males (van Schaik et al., 1999).
Paternity confusion should affect the evolution of
dimorphism by tempering the effect of male-male
competition on differential male reproductive suc-
cess, but the magnitude of such an effect may be
extremely difficult to measure. While multiple mat-
ings might confuse paternity, they do not mean that
male dominance has no benefit to males. For exam-
ple, Nunn (1999) hypothesized that exaggerated es-
trous swellings in female catarrhines serve as grad-
ed signals of female fertility in multimale groups.
In this model, females prefer to mate with the dom-
inant male at the time most likely to result in fer-
tilization, but also want to confuse paternity to
guard against infanticide. Dominant males guard
females at maximum tumescence only, allowing
other males to mate with the female at other points
in her cycle. However, there is not an exact corre-
spondence between ovulation and maximum tumes-
cence. Hence, while the dominant male has the
greatest chance of siring offspring, other males will
also have a chance of siring offspring, thereby con-
fusing paternity. If true, then female choice counters
male infanticide, and both dampens and maintains
differential male reproductive success resulting
from agonistic competition.
A more recent hypothesis is that female primates
regulate group size in order to avoid infanticide
risks (Pope, 2000). In this model, the probability of
male takeover of a group is proportional to group
size. Because infanticide usually follows a male
takeover, females may evict other females in order
to keep group size down. If true, this might limit
differential male reproductive success by limiting
the number of females that a male can monopolize,
hence limiting selection for the development of
weaponry. At the same time, such agonistic encoun-
[Vol. 44, 2001
ters between females could possibly select for larger
female canines, further reducing dimorphism.
Finally, females may seek dominant males for pro-
tection from infanticidal males (Sterk, 1997; Kap-
peler, 1999). In single-male species, infanticide fol-
lows male takeover of a group. Hence, association
with a dominant male may help protect female off-
spring from infanticidal males, and may be a pri-
mary factor in the formation of groups in some spe-
cies. It is tempting to speculate that extreme body
size dimorphism in gorillas reflects differential male
reproductive success that is enhanced or driven by
strong female choice.
Models for other causes of dimorphism
As noted above, the importance of factors other
than sexual selection on dimorphism has been long
debated. While recent studies have corroborated and
elaborated the importance of sexual selection and
intrasexual competition in the evolution of dimor-
phism, they have also confirmed the complexity of
forces that drive or constrain the evolution of dimor-
phism. Dimorphism in various traits is known to be
correlated with body mass, diet, substrate, phylog-
eny, and even rainfall. Each of these correlations
may reflect a variety of different mechanisms affect-
ing the expression and evolution of dimorphism.
Body size. Sexual dimorphism in body mass and
canine tooth size is correlated with overall body size
(Clutton-Brock et al., 1977; Harvey et al., 1978; Leu-
tenegger and Cheverud, 1982, 1985; Gautier-Hion
and Gautier, 1985; Cheverud et al., 1985; Plavcan
and van Schaik, 1992, 1994, 1997b; Pickford, 1986;
Plavcan, 1999). This phenomenon has been docu-
mented across a wide variety of animals (Rensch,
1960), and remains a topic of much discussion (Re-
iss, 1986; Andersson, 1994; Fairbairn, 1997). The
model of Leutenegger and Cheverud (1982, 1985)
explained this as a function of greater male charac-
ter variability, but, as previously reviewed, their
analysis has been subject to much criticism.
Other mechanisms may explain the correlation.
Clutton-Brock et al. (1977) suggested five mecha-
nisms that might explain the relationship: 1) Selec-
tion for larger male size might also favor larger
female size as a correlated response. 2) At large
size there are fewer competing species, freeing
males to increase size without facing ecological com-
petition. 3) It may be energetically cheaper to in-
crease male body size at larger sizes. 4) Selection
may favor size differences to reduce feeding compe-
tition at larger sizes, if larger species tend to feed on
low-density food distributed in clumps. 5) There
might be greater pressure to reduce female body size
at larger sizes in order to speed female maturation
so that they can breed at a younger age. Kappeler
(1990, 1991) suggested that the lack of mass dimor-
phism in strepsirrhines might be explained if, at
smaller body size, selection favors speed and agility
over increase in male body mass or canine tooth size.
J.M. Plavcan] DIMORPHISM IN PRIMATES
Other studies suggest that there may be a causal
relationship between body size and sexual selection.
At larger body sizes, females tend to form large
groups, which makes it easier for males to try to
exclude other males from access to females. Mitani
et al. (1996) noted that their estimate of the opera-
tional sex ratio is significantly correlated with body
mass, while Plavcan and van Schaik (1997b) noted
that competition levels are also correlated with body
size. Unfortunately, all of these models are contra-
dicted by the observation that small (1,000 g) early
anthropoids were sexually dimorphic in body size
(Simons et al., 1999). This suggests that no current
model satisfactorily explains the link between size
and dimorphism in living primates.
The mechanism underlying the correlation be-
tween size and dimorphism has strong implications
for the way that dimorphism should be measured in
comparative analyses. If dimorphism is a direct
function of increasing body size, then it is appropri-
ate to measure relative dimorphism as a residual
from a regression of dimorphism against body size
(e.g., Ford, 1994; Mitani et al., 1996). Allometric
adjustment of dimorphism assumes that there is a
nonadaptive baseline of dimorphism contingent on
size, with sexual selection modifying the expression
of dimorphism. However, if dimorphism covaries
with body size through an interaction between body
size and female grouping pattern, sexual selection,
and male mating competition, then regression of
dimorphism against size will remove the correlation
between sexual selection and dimorphism, inappro-
priately biasing against corroboration of the sexual
selection hypothesis. Unfortunately, allometric re-
gression of dimorphism is too often taken as a given,
with little attention given to the underlying assump-
tions. Recent comparative analyses (Kappeler, 1990,
1991; Godfrey et al., 1993; Mitani et al., 1996; Plav-
can and van Schaik, 1997b; Plavcan, 1999) suggest
that the adage that correlation does not equal cau-
sation needs to be heeded in this case, and allomet-
ric adjustment of dimorphism should be avoided
without careful justification. Rather, attention
should be directed first to testing hypotheses about
the causal relationships between dimorphism, size,
behavior, and ecology.
Diet. Several studies have suggested that body
mass dimorphism is linked to diet. Leutenegger and
Kelly (1977) and Milton (1985) suggested that a
low-energy, folivorous diet may constrain either the
expression of dimorphism, or male-male competi-
tion. Conversely, Ford (1994) and Mitani et al.
(1996) suggested that a folivorous diet might allow
males to become larger, leading to enhanced mass
dimorphism.
Diet is only weakly associated with variation in
dimorphism in that folivorous species tend to be less
dimorphic than other species. However, this rela-
tionship is very loose: proboscis monkeys and goril-
las are folivorous, and are among the most dimor-
41
phic catarrhines, while folivorous howler monkeys
are the most dimorphic platyrrhines. Correlations
between diet and either canine or body mass dimor-
phism are not significant in controlling for male-
male competition levels (Plavcan and van Schaik,
1992, 1994, 1997b). The idea that male-male compe-
tition might be less intense in folivorous species
through an energetic constraint (Leutenegger and
Kelly, 1977; Milton, 1985) is contradicted by the
intense male-male competition seen in some foli-
vores (e.g., Presbytis thomasi, Procolobus verus, Go-
rilla gorilla; Plavcan and van Schaik, 1997b). Alter-
natively, females of folivorous species tend to be
more dispersed in association with scramble com-
petition, possibly limiting male differential repro-
ductive success (Plavcan and van Schaik, 1994), but
this idea is difficult to test, and again fails to explain
the strong dimorphism of some folivorous species.
Thus, the weight of evidence suggests (albeit incon-
clusively) that diet is not an important factor di-
rectly affecting the evolution of dimorphism.
Careful scrutiny reveals that, controlling for esti-
mates of male-male competition, the only folivorous
anthropoids that show usually weak body mass di-
morphism are colobines. Interestingly, many folivo-
rous colobines also show strong canine dimorphism
(Plavcan and van Schaik, 1997b). The strong canine
dimorphism and intense male-male competition
suggest that sexual selection operates in these ani-
mals as in other anthropoids. This in turn suggests
that the lack of mass dimorphism could reflect a
situation where body mass either is no longer im-
portant in determining the outcome of fights, or is a
constraint on the evolution of body mass dimor-
phism. It is interesting to note that large folivorous
species (gorillas and proboscis monkeys) tend to
show intense body mass dimorphism, whereas
smaller folivorous species do not. Perhaps there is a
balance between pressure to limit body mass in as-
sociation with locomotion (see below), and to in-
crease it in order to slow gut-passage time in order
to make digestion more efficient. Hence, low body
mass dimorphism may reflect pressure to maximize
female body mass in smaller folivorous species. Con-
versely, the dissociation might reflect an interaction
between feeding, locomotion, and substrate use.
Colobine primates tend to be leapers exploiting
leaves and fruits on small branches, and they tend to
be large. Hence, there may be a constraint on colo-
bine male body size that limits the expression of
body mass dimorphism (Leutenegger and Kelly,
1977).
Greenfield (1992a, 1998) suggested that canine
tooth size reduction, and hence reduction in canine
tooth size dimorphism, reflects pressure to incorpo-
rate the canine teeth into an incisal functional field.
Greenfield (1992a, 1998) noted that the develop-
ment of the mesial cristid on the mandibular canine,
which occludes with the lateral maxillary incisor in
many anthropoids, is inversely correlated with man-
dibular canine crown height. He suggested that de-
42 YEARBOOK OF PHYSICAL ANTHROPOLOGY
velopment of this contact is the primary driving
force behind canine reduction in anthropoid pri-
mates. Plavcan and Kelley (1996) noted that while
the mesial cristid may reflect a functional contact,
the hypothesis does not necessarily explain maxil-
lary canine reduction: strepsirrhine primates com-
pletely incorporate the mandibular canine into a
functional incisal field (in this case, the tooth comb),
without concomitant reduction of the maxillary ca-
nine. In fact, they redevelop the mandibular P2 to
function as a canine. This demonstrates that func-
tional alterations (be they dietary or otherwise) of
the mandibular canine need not dictate any reduc-
tion of the maxillary canine.
There is one clear case of a dietary effect on canine
dimorphism. Pithecine primates use their canine
teeth to open hard fruit (Kinzey, 1992). The canines
of both sexes are enlarged and modified to look like
chisels. Canine dimorphism in pithecines species is
modest or absent, undoubtedly reflecting this di-
etary specialization (Greenfield, 1992a,b, 1998;
Plavcan and Kelly, 1996).
In summary, there is only very weak evidence for
a causal relationship between dimorphism and diet
in primates. No mechanism (energetic constraints,
metabolic constraints, association between diet and
female dispersal patterns, locomotor constraints, or
selection to turn canines into incisors) adequately
explains the very weak correlation between diet and
dimorphism seen across all anthropoids. While this
does not rule out an important role for diet in the
evolution of dimorphism, it suggests that any such
role is secondary to the effects of sexual selection.
On the other hand, dietary specialization of the ca-
nine teeth clearly affects canine dimorphism in some
species.
Terrestriality. It is well-known that terrestrial
species tend to be more dimorphic than arboreal
species (Crook, 1972; Clutton-Brock et al., 1977;
Harvey et al., 1978; Leutenegger and Kelly, 1977;
Gaulin and Sailer, 1984; Cheverud et al., 1985; Gau-
tier-Hion and Gautier, 1985; Plavcan and van
Schaik, 1992, 1994, 1997b; Martin et al., 1994). This
is commonly thought to reflect greater predation
pressure on terrestrial species, assuming that they
are more susceptible to predators than arboreal spe-
cies. If male primates are more susceptible to pre-
dation, either because they spend greater periods of
time alone, or because they more frequently defend
groups against predators, then larger size and
larger canine teeth should be favored. Plavcan and
van Schaik (1992) noted that savanna-dwelling spe-
cies are more dimorphic than forest-dwelling species
of the same competition levels, supporting this hy-
pothesis. However, there are other reasonable expla-
nations. For example, there is the hypothesis that
arboreal species face an upper body size limit: larger
body size should constrain arboreal species from
moving about the trees, especially on smaller sub-
strates (Clutton-Brock et al., 1977; Leutenegger and
[Vol. 44, 2001
Kelly, 1977). Female group size may be larger in
more terrestrial species, leading to greater male-
male competition. Alternatively, females may be
easier to guard in a two-dimensional, open habitat
than in a three-dimensional closed habitat. Such
hypotheses are difficult to prove, but the consistency
of the observation strongly suggests that some
mechanism associated with substrate use constrains
or enhances dimorphism.
Correlated response. Correlated response is an-
other factor that can influence the expression of
dimorphism. Correlated response is the phenome-
non whereby a character that is functional in one
sex appears in the other because the genes for the
trait are not located on the sex chromosomes (Lande,
1980). In other words, if the genes determining a
trait are not located on the sex chromosomes, then
selection that favors a change in the trait in one sex
should automatically produce the same change in
both sexes. Lande (1980) showed that if selection
favors the trait in one sex, but that the trait is
disadvantageous in the other sex, then selection
should favor some mechanism to decouple the ex-
pression of the trait between sexes. However, the
time necessary for this could be quite long.
The phenomenon is particularly interesting be-
cause the model predicts that dimorphism will
evolve by the reduction of a trait in one sex. For
example, selection may have initially favored the
development of large male canines in the ancestral
anthropoid, producing large canines in both sexes.
Canine dimorphism would then have evolved if large
canines are somehow disadvantageous in females,
producing selection favoring a decoupling of genetic
control of male and female tooth size, and reduction
in female canine size.
Greenfield (1992a, 1998) attributes variation in
anthropoid female canine size primarily to corre-
lated response. Female relative canine size is corre-
lated with male relative canine size across all an-
thropoids (Greenfield, 1992a, 1998; Plavcan et al.,
1995; Plavcan, 1998). Plavcan (1998) demonstrated
that this relationship only holds across species in
which females show little or no agonistic competi-
tion. In those species showing female agonistic com-
petition, there is no correlation between relative
male and female canine size. This suggests that
correlated response affects female canine size, but
does not constrain the evolution of large female ca-
nine size in association with agonistic competition.
Greenfield (1996) presented evidence that corre-
lated response may affect the development of the
honing premolars in female anthropoid primates,
which appear to be larger than necessary to accom-
modate the maxillary canine in many anthropoid
species. Correlated response may influence other an-
atomical characters in primates, but unfortunately
the mechanism has received little attention beyond
that just mentioned.
J.M. Plavcan] DIMORPHISM IN PRIMATES
Niche divergence. There has long been specula-
tion that niche divergence favors the evolution of
size dimorphism in primates (Clutton-Brock et al.,
1977). The concept is derived from studies of birds,
which have shown that males and females some-
times differ in both size and diet, apparently to
reduce feeding competition between the sexes. There
have been some indications that male and female
diets differ in orangutans and some other species.
However, dietary differences tend to be relatively
slight, and the niche divergence hypothesis has
never received much support. At least part of the
problem is that it is very difficult to tease apart the
causes of dietary differences between males and fe-
males, and it is almost impossible to determine if
any dietary differences drive the evolution of dimor-
phism, or whether dimorphism itself produces di-
etary differences.
More intriguing is the suggestion that body mass
dimorphism in part reflects selection for reduced
female body mass in association with dietary con-
straints (Demment, 1983; Martin et al., 1994). Fe-
male primates spend a significant portion of their
adult lives pregnant or lactating, both of which rep-
resent significant metabolic commitments by fe-
males. It has been suggested that, metabolically,
female body size really should be measured as the
sum of the females body mass along with that of her
fetal or suckling offspring (Demment, 1983; Smith
and Jungers, 1997). If true, then body mass dimor-
phism of many species might partly reflect a reduc-
tion in female body mass in order to compensate for
the demands of pregnancy and lactation. Of course,
if this hypothesis were universally true, then we
would have trouble explaining monomorphism. One
test might be to compare seasonality or resource
availability during the pregnancy and lactation of
species showing similar mating systems, predicting
that size dimorphism should be greater in environ-
ments with less abundant resources. Of course, the
difficulty in doing this is accurately estimating the
strength of sexual selection.
Taxonomy. Dimorphism is strongly correlated
with phylogeny (Cheverud et al., 1985; Leutenegger
and Lubach, 1987; Martin et al., 1994; Plavcan and
van Schaik, 1994, 1997b). I have already touched on
the pattern of weak mass dimorphism and strong
canine dimorphism in colobines, but other taxo-
nomic groups exhibit characteristic patterns of di-
morphism (Table 1). For example, papionines are all
strongly dimorphic, and most have exaggerated fe-
male estrous swellings. Callitrichine primates all
exhibit low levels of dimorphism coupled with either
monogamous or polyandrous mating systems. All
hylobatids are monogamous and show low levels of
dimorphism. The list can go on for different combi-
nations of characters at different taxonomic levels.
Cheverud et al. (1985) demonstrated that a large
part of the variation in anthropoid body mass dimor-
phism is explained (statistically) by phylogeny. In
43
other words, they suggested that a species shows a
particular degree of dimorphism because its ances-
tor was dimorphic.
Phylogenetic constraint is sometimes used to ex-
plain phylogenetic correlations of characters. But
the term is ill-defined, and seems unsatisfactory as
an explanation unto itself because it does not neces-
sarily specify any particular mechanism, apart from
the fact that there is a correlation between a trait
and phylogeny. However, as far as dimorphism goes,
operational sex ratios, mating systems, modes of
locomotion, substrate preference, diet, and habitat
preference are also correlated with phylogeny (Clut-
ton-Brock et al., 1977; Harvey et al., 1978; Mitani et
al., 1996; Plavcan and van Schaik, 1997b; Plavcan,
1999). This raises the question of what, exactly,
underlies such phylogenetic correlations? Do they
reflect genetic constraints on the expression of char-
acters, historical baggage from an ancestral condi-
tion, or canalized evolution reflecting a compromise
in the expression of multiple characters? These
questions are extremely difficult to tease apart.
It has been suggested that dimorphism in Simias
concolor and Cercopithecus neglectus are examples
of phylogenetic inertia, on the basis that both spe-
cies are monogamous (Leutenegger and Lubach,
1987). In these cases, dimorphism is hypothesized to
reflect a condition held over from an ancestor that
was probably polygynous. One can imagine a num-
ber of hypotheses to explain the phenomenon: either
selection has not had time to reduce dimorphism (an
evolutionary time lag), selection cannot alter the
magnitude of dimorphism (because of some develop-
mental or genetic constraint on changes in male or
female body size relative to each other), or perhaps
there is no selective pressure to alter the degree of
dimorphism. However, while observations of male-
female pairs are not doubted, Watanabe (1981)
showed convincingly that S. concolor is monoga-
mous only in areas subject to hunting pressure.
Other reports also suggest that C. neglectus is not
monogamous throughout its range (Brennan, 1985).
This suggests that these two species might not be
clear cases of phylogenetic constraint.
One of the most puzzling taxonomic patterns of
dimorphism is that between prosimians and anthro-
poids. Strepsirrhines and tarsiers exhibit little or no
sexual dimorphism in body mass, tooth size, or pel-
age, while anthropoids commonly exhibit extreme
levels of dimorphism in one or more of these char-
acters. Yet both groups are characterized by polyg-
yny and intense male-male competition in many
species. Kappeler (1991) suggested that strepsir-
rhines exhibit little dimorphism because selection
favors fighting skills and agility rather than weap-
onry. Plavcan et al. (1995) noted that male and
female strepsirrhines tend to exhibit similar types of
intrasexual competition, and suggested that the lack
of dimorphism reflects similar selection pressures
for the development of weaponry and size in males
and females. Plavcan (1998) suggested that corre-
44 YEARBOOK OF PHYSICAL ANTHROPOLOGY
lated response may explain the lack of canine dimor-
phism in strepsirrhines, though he noted that the
equal male/female competition hypothesis of Plav-
can et al. (1995) was still a viable explanation. Leigh
and Terranova (1998) suggested that body mass di-
morphism is constrained in Malagasy lemurs as a
consequence of extreme seasonality in resource-poor
environments. All of these hypotheses are reason-
able, supported by data, and difficult to disprove.
In summary, it is now well-established that there
are strong phylogenetic correlations in dimorphism
as well as the behavioral/ecological variables that
are hypothesized to be causally linked to the evolu-
tion of dimorphism. The reasons for phylogenetic
correlations in all these variables are likely to vary.
The evolution of phylogenetic patterns is itself in
need of study. But regardless of the reasons under-
lying the existence of these patterns, the strength of
phylogenetic correlations mandates that compara-
tive analyses testing for general causal mechanisms
of dimorphism across taxonomic groups must care-
fully control for phylogenetic correlations in the
data, using modern comparative methods (e.g.,
Cheverud et al., 1985; Pagel, 1994; Plavcan and van
Schaik, 1994; Plavcan et al., 1995; Mitani et al.,
1996; Nunn, 1999).
Epiphenomenal variation. An often unappreci-
ated factor contributing to sexual dimorphism is
epiphenomenal variation. This is variation that re-
sults from different environmental conditions which
might affect growth and development, or even from
local adaptation in subspecies of a widely spread
species. Populations and subspecies can differ in
dimorphism from one to another. Turner et al.
(1994, 1997) demonstrated that Cercopithecus ae-
thiops populations from different parts of Kenya
differed significantly in body mass dimorphism,
largely as a result of changes in female body mass.
Females from areas showing higher average rainfall
showed greater body mass than those from drier
areas. More recently, Jones et al. (2000) presented
evidence that Alouatta palliata subspecies differ in
the magnitude and pattern of sexual dimorphism,
though the cause of this variation is unclear.
On a larger scale, Hayes et al. (1995) demon-
strated variation in dimorphism and relative female
canine tooth size in Colobus guereza. Guereza mon-
keys are peculiar in that females can possess enor-
mous canine teeth. Variation in relative female ca-
nine size among guereza populations is very high.
Clearly, canine tooth size sexual dimorphism in this
species varies as a function of variation in female
canine size. The reason for this variation has been a
continuing mystery. Hayes et al. (1995) noted that
females from drier environments had significantly
larger canines than those from wetter habitats.
They suggested that predation pressure favors large
female canines. Seed predation may be another ex-
planation (with females using their canines to open
hard fruit, as in pithecine primates), or higher levels
[Vol. 44, 2001
of intrasexual competition. Unfortunately, there is
not enough comparative evidence to make any judg-
ment about female agonistic competition. Female
guerezas do eat seeds, but so do other colobines.
Likewise, other anthropoid primates live in dry hab-
itats, with females susceptible to predation, and
there is little actual documentation of predation or
predator defense among guereza subspecies. Re-
gardless of the cause, the variation in canine dimor-
phism among guereza subspecies is real and signif-
icant.
ONTOGENY
Most studies of sexual dimorphism focus on adult
characters. However, sexual dimorphism in adults is
necessarily a product of different male and female
growth trajectories. Shea (1986) pointed out that
males can get larger than females either by extend-
ing a common growth trajectory and maturing later
than females (time hypermorphosis or bimatur-
ism), or by growing faster than females in a given
period of time (rate hypermorphosis). Likewise,
dimorphism can be produced if females mature ear-
lier than males, or grow more slowly.
Leigh (1992) documented and quantified patterns
of growth in males and females of 38 primates, dem-
onstrating convincingly that size dimorphism arises
through variation in both time and rate hypermor-
phosis. Most species showed some combination of
both bimaturism and sex differences in growth rate.
Most interesting was the fact that congeneric spe-
cies could vary in the pattern of development lead-
ing to a particular degree of sexual dimorphism.
While adults of two closely related species might
show the same magnitude of body mass dimorphism,
one might achieve it through extended male growth,
while the other might achieve it through rate hyper-
morphosis. Clearly, the magnitude of adult mass
dimorphism in a species is not constrained by the
ontogenetic pattern of dimorphism, but this raises
the question of why species should differ in the pat-
tern of male and female development.
Leigh (1995b) suggested that males can follow
alternate developmental pathways as a response to
selection pressure faced by juveniles. He found that
most species in which adult dimorphism is achieved
through rate hypermorphosis live in single-male
groups, while those that achieve adult dimorphism
through time hypermorphosis tend to live in multi-
male groups. Leigh (1995b) suggested that this ob-
servation is consistent with two models: juvenile
risk aversion (Janson and van Schaik, 1993), and
social complexity.
Janson and van Schaik (1993) pointed out that
primates can be roughly divided into those that pur-
sue a fast life-history, in which development is
accelerated, and those that pursue a slow life-his-
tory, in which development is prolonged. The juve-
nile risk aversion model posits that rapid rates of
growth are associated with higher mortality in pri-
mates, probably as a result of competition with
J.M. Plavcan] DIMORPHISM IN PRIMATES
adults. For male primates growing up in multimale
groups, a slow rate of growth will minimize compe-
tition with adults, both for food resources, and by
extending the period during which adult males do
not view juveniles as competitors for mates. Con-
versely, males from single-male groups are usually
evicted from a group relatively early. This subjects
the male to greater risks, favoring rapid attainment
of large body size.
The social complexity model posits a basic differ-
ence in social complexity between single-male and
multimale groups (Leigh, 1995b). The model as-
sumes that in order to reproduce successfully, males
growing up in multimale groups need longer periods
of time to learn the social skills necessary to interact
with and form social bonds with both adult males
and females. Such males normally experience a
short period alone when they transfer from their
natal troop to a new troop. Before and after transfer,
the male experiences an extended period of time in
which it is low in the resident dominance hierarchy.
Essentially, these males can afford a period of time
during which they can increase in size, gain experi-
ence, develop social skills, form alliances, and even-
tually move up the dominance hierarchy to achieve
reproductive success. In contrast, males living in
single-male groups are evicted from their natal
troop when they become juveniles, and spend an
extended period of time either alone, or with a band
of other young males. Males may take over a troop of
females, during which time they can monopolize
access to a group of females. Once evicted from their
natal troop, their chances of successfully taking over
another troop are low. Hence, long-term bonds with
other individuals and social skills are not as impor-
tant to these animals in gaining access to females.
Of course, both of these descriptions oversimplify
the variety of social relationships seen among pri-
mates, but the generalization seems to have some
power. However, Leigh (1995b) notes that limited
comparisons find no real difference in age of male
maturity between multimale and single-male spe-
cies, even though there are substantial instanta-
neous differences in growth rates during ontogeny.
Leigh (1995b) suggests that detailed evaluations of
growth rate differences during ontogeny are neces-
sary to completely evaluate both models.
Leigh and Shea (1995) provided a detailed com-
parison of growth, body mass dimorphism, and be-
havioral ecology in living hominoids. They suggested
that orangutan males show an indeterminate in-
crease in body mass (they could demonstrate no
point at which males ceased increasing in body
mass), and gorillas and Pan paniscus achieve size
dimorphism largely through bimaturism, while P.
troglodytes achieves it through an increase in the
rate of male growth. More importantly, they noted
that both species of Pan show similar levels of adult
dimorphism, but they achieve it through different
patterns of male and female development. Pan pa-
niscus females show early maturation relative to P.
45
troglodytes females. Likewise, gorilla females ma-
ture early, enhancing the magnitude of dimorphism.
This strongly implies that changes in the female
pattern of growth constitute an important compo-
nent in the final magnitude of dimorphism.
Leigh and Shea (1995) suggested that female
growth trajectories are strongly linked to diet. Again
referring to the model by Janson and van Schaik
(1993) of juvenile risk aversion, they suggested that
female growth patterns are strongly influenced by
female competition over resources. Janson and van
Schaik (1993) suggested that species engaging in
contest competition over resources (largely associ-
ated with frugivorous diets, wherein resources are
patchily distributed) will face greater juvenile risks
at faster growth rates, as a result of competition
with adults over limited resources. In contrast, spe-
cies characterized by scramble competition (largely
associated with folivorous diets) will not face in-
creased juvenile risks at high growth rates, because
of an abundance of scattered resources. Leigh and
Shea (1995) suggested that in this latter case, selec-
tion can favor rapid female maturation and an ear-
lier start to reproduction without increasing female
juvenile mortality. Hence, gorillas and Pan panis-
cus, which are characterized by scramble competi-
tion, show early female maturation (and smaller
body size), while P. troglodytes, which is character-
ized by female contest competition, prolongs female
maturation in order to minimize juvenile risks. Im-
portantly, Leigh and Shea (1995) also note the major
contribution of sexual selection through male-male
competition to adult dimorphism. Thus, the final
magnitude of adult dimorphism is a sum of selection
on males and females.
On the basis of indirect evidence, Martin et al.
(1994) suggested that body mass dimorphism among
anthropoid primates is primarily a consequence of
reduced female body mass through early matura-
tion. They noted that brain size and molar tooth size
are determined early in development, and tend not
to be dimorphic. They then predicted that if dimor-
phism is a function of extended male growth, then
males of dimorphic species should have relatively
small brains and teeth by comparison to monomor-
phic species. They presented evidence that in fact
females of dimorphic species have relatively large
brains and teeth, suggesting a reduction in female
body size. Their conclusion was partly based on the
observation of a failure to find a relationship be-
tween body size dimorphism and male-male compe-
tition. Since that time, however, Ford (1994), Mitani
et al. (1996), and Plavcan and van Schaik (1997b)
demonstrated such a relationship. Nevertheless,
there is no reason that the observation might not be
valid, and the hypothesis needs to be explored in
greater detail.
The results of these studies both complement and
contrast with those of Plavcan et al. (1995) on rela-
tive male and female canine size. All studies clearly
demonstrate that dimorphism is a function of
46 YEARBOOK OF PHYSICAL ANTHROPOLOGY
changes in male and female characters. Leigh and
Shea (1995) and Plavcan et al. (1995) both associate
female contest competition with changes in dimor-
phism. However, Plavcan and van Schaik (1995)
associate noncoalitionary female contest competi-
tion with decreased canine dimorphism through se-
lection for enhanced female weaponry. In contrast,
Leigh and Shea (1995) associate this type of compe-
tition with reduced dimorphism through prolonged
female growth associated with reduction of female
mortality. Hence, the effects of contest competition
on canine and body size dimorphism are parallel,
but the underlying mechanisms are very different.
Leigh and Shea (1995) and Leigh and Terranova
(1998) both suggested that the absence of body mass
dimorphism in living strepsirrhine primates reflects
a constraint on growth trajectories due to extreme
seasonality. Leigh and Terranova (1998) pointed out
that polygynous malagasy lemurs experience very
rapid rates of growth. At the same time, these ani-
mals live in highly seasonal environments and are
forced to resort to low-quality resources during part
of the year. This places a premium on rapid body-
size increase. The highly restricted breeding season
may also select strongly for a limit on the timing of
male maturation. Hence, the combination of pres-
sure for rapid growth and early maturation may
limit the ability of males to achieve larger size than
females by constraining bimaturism, and capping
growth rates in both males and females.
Finally, work has recently begun comparing
growth rates of canine teeth between male and fe-
male primates. Schwartz and Dean (2001) demon-
strated that canine dimorphism in living hominoids
is a function of time hypermorphosis. Male canines
tend to grow for longer periods of time than those of
females, but not at a different rate. Though their
comparative sample was small, the results are in-
triguing. It will be interesting to compare rates of
female canine development between species show-
ing different relative female canine sizes.
In sum, there is a growing literature on the ontog-
eny of dimorphism which promises to shed consid-
erable light on the different mechanisms by which
animals achieve dimorphism. These studies have
demonstrated that the magnitude of adult dimor-
phism reflects any one of a combination of extended
male growth, shortened female growth, more rapid
male growth, or slower female growth. It is interest-
ing to note that the magnitude of adult dimorphism
is not contingent on any particular growth path: two
species can share the same level of dimorphism in
adults that is achieved through different combina-
tions of male and female growth trajectories. This
suggests that sexual selection favoring adult dimor-
phism works in concert with, and not against, dif-
ferent selective pressures on juvenile growth trajec-
tories. There is growing evidence that different
ontogenetic pathways reflect different selective
pressures on males and females. Males might alter
developmental pathways in association with differ-
[Vol. 44, 2001
ent types of juvenile risks, or as a function of male
social strategies. Females may alter growth patterns
as a function of dietary pressures, and/or as a func-
tion of pressure for altering reproductive rates.
DIMORPHISM IN THE FOSSIL RECORD
Dimorphism in the primate fossil record
Knowledge about dimorphism in the fossil record
can be valuable for both species recognition and
reconstruction of social behavior. In the first place,
sexual dimorphism can be a source of variation in a
morphological sample. Where the sex of individual
specimens cannot be reliably determined, sexual di-
morphism can mimic interspecific variation (Gin-
gerich and Schoeninger, 1979; Cope, 1993; Plavcan,
1993b; Plavcan and Cope, 2001). This has been a
particular problem for those interested in human
evolution, where the question of two sexes or two
species has been a focus of controversy (e.g., Zihl-
man, 1985; Cole and Smith, 1987; Leutenegger and
Shell, 1987; Kimbel and White, 1988; Miller, 1991,
2000; Wood, 1993; Kramer et al., 1995; Richmond
and Jungers, 1995; Lockwood et al., 1996; Lockwood,
1999). In the second place, the association between
sexual dimorphism and male-male competition and
mating systems means that it has often served as
the only direct evidence for social behavior in the
fossil record (e.g., Wolpoff, 1976; Fleagle et al., 1980;
Gingerich, 1981, 1995; Lovejoy, 1981; Leutenegger
and Shell, 1987; Foley and Lee, 1989; Kelley, 1989;
Krishtalka et al., 1991; McHenry, 1994a,b; Plavcan
and van Schaik, 1997a; Simons et al., 1999; Plavcan,
2000a).
Apart from this, a survey of what is known about
sexual dimorphism in the fossil record reinforces
and expands our knowledge of the causes and ex-
pression of dimorphism in primates. Evidence from
the fossil record demonstrates that dimorphism (and
therefore probably polygyny): 1) arose early in an-
thropoid evolution and at small body sizes (Simons
et al., 1999); 2) has arisen independently in different
primate lineages (Krishtalka et al., 1991); and 3) in
a number of species probably substantially exceeded
that observed in the most dimorphic living primates
(Kelley and Xu, 1991; Kelley and Plavcan, 1998).
Catopithecus and Proteopithecus provide the ear-
liest evidence of sexual dimorphism in the anthro-
poid fossil record so far (Simons et al., 1999). Both of
these early anthropoids were small (substantially
less than 1,000 g), demonstrating that the evolution
of sexual dimorphism itself is not a function of the
evolution of large body size. This is reinforced by the
observation that Apidium, another small, slightly
younger early anthropoid, was strongly dimorphic
(Fleagle et al., 1980). The presence of sexual dimor-
phism in these species implies polygyny, suggesting
that high operational sex ratios and male-male com-
petition are not a function of the evolution of large
size (Simons et al., 1999), and that the correlation
between body mass and sexual dimorphism in living
J.M. Plavcan] DIMORPHISM IN PRIMATES
primates reflects the absence of strongly polygy-
nous, small-bodied, living anthropoids. Why such
species are absent today is an interesting question,
but small size alone is not the reason.
The correlated response model discussed above
makes a clear prediction about the evolution of di-
morphism in early primates. If this model is true,
then it implies two things about dimorphism in early
anthropoids. First, the earliest anthropoids, or their
immediate ancestors, may have been characterized
by large canine teeth in both sexes, if the primitive
condition for preanthropoid primates was small ca-
nines in both sexes, coupled with solitary habits.
Paleocene mammals such as Purgatorius came
equipped with small canine teeth in both sexes, sup-
porting the hypothesis that canines were small in
the ancestral primates, while other evidence sug-
gests nocturnality and therefore probably solitary
habits in the ancestral primate (Ross et al., 1998). If
true, an increase in canine size in both sexes, and
not the appearance of canine dimorphism, should
have accompanied the evolution of polygyny in the
earliest anthropoids. This implies, in turn, that the
evolution of dimorphism would have lagged behind
the evolution of polygynous mating systems. In this
model, monomorphism resulting from big canines in
both sexes would not be indicative of monogamy or
polyandry.
The second implication is that the evolution of
canine dimorphism in primates may have arisen
through a reduction in female canine size. If so, then
the emergence of canine dimorphism in early an-
thropoids should track the dissociation of genetic
control over male and female canine size, and should
indicate not an increase in male-male competition,
but a decrease in female-female competition. All this
is speculative. However, given the rapid increase in
the number of Eocene primates being discovered in
Asia and Africa, it provides an interesting basis for
interpreting the meaning of the evolution of canine
teeth in these animals.
There is evidence of dimorphism in Eocene adapid
primates. Cantius and Notharctus both were char-
acterized by sexually dimorphic canine teeth, and
possibly substantial body mass dimorphism (Gin-
gerich, 1981, 1995; Krishtalka et al., 1991). There
has long been an argument over whether living an-
thropoids arose from or are the sister taxon of either
Eocene adapids or omomyids. Current models for
anthropoid origins suggest that living tarsiers are
the extant sister taxon of anthropoids, to the exclu-
sion of strepsirrhines, and that omomyids are the
sister taxon of anthropoids from the Eocene, to the
exclusion of adapids (Ross et al., 1998). If adapids
did not give rise to anthropoids, then sexual dimor-
phism has clearly evolved more than once within
primates. Furthermore, if adapids are ancestral to,
or the sister taxon of, living strepsirrhines, then the
lack of dimorphism in this extant group may not
reflect a direct genetic constraint on the expression
of dimorphism. On the other hand, the presence of
47
sexual dimorphism in early adapids has been used
as evidence for an adapid origin for anthropoids
(Covert and Williams, 1994). Given that dimorphism
has arisen independently in carnivores, ungulates,
pinnipeds, macropods, primates, cetaceans, and nu-
merous other vertebrate and invertebrate groups, it
would not be surprising that the character has
arisen independently in different primate lineages.
The variability in the magnitude of the character
among extant anthropoids would suggest that the
simple presence of dimorphism alone constitutes
only weak evidence for a link between anthropoids
and adapids.
Sexual dimorphism has been documented in most
later anthropoid taxa, including oligopithecids,
parapithecids, early catarrhines, most hominoids,
and early hominids (Ross et al., 1998, provide a
tabular summary). Miocene apes offer one of the
most intriguing pictures of sexual dimorphism, first
because they demonstrate unique aspects of dimor-
phism not seen in living species, and second because
the ancestral hominid condition presumably arose
from a Miocene ape pattern. Dimorphism appears to
be common among Miocene apes, most of which dis-
play large, easily recognizable male canine teeth
and substantial size dimorphism (Kelley, 1986,
1993, 1995a; Kelley and Xu, 1991).
Highly intriguing is the likelihood that a number
of Miocene hominoids were more dimorphic than
any living primate. The most extreme example is
Lufengpithecus. The hominoid dental samples from
Lufeng, China, are highly variable. It has been sug-
gested that this reflects the presence of two species
at the site (Wu and Oxnard, 1983a,b; Martin, 1991;
Cope and Lacy, 1992, 1994; Plavcan, 1993b). How-
ever, others maintain that the sample is composed of
a single, extremely dimorphic species (Wu, 1987;
Kelley and Etler, 1989; Kelley and Xu, 1991; Wood
and Xu, 1991; Kelley, 1993). Most recently, Kelley
and Plavcan (1998) demonstrated that the pattern of
metric variation in the sample is most consistent
with the presence of a single species more dimorphic
than any living hominoid. The extreme dimorphism
of Lufengpithecus opens up the possibility that apes
from other Miocene localities were also so character-
ized. This leads to the question of what drove such
extreme dimorphism. Was it extreme sexual selec-
tion? Perhaps there was selection to reduce female
body size. Perhaps there was some relaxation of
constraints on male body size, allowing runaway
evolution of large male size. Perhaps males differed
ecologically from females. Unfortunately there is no
way to eliminate most hypotheses with current in-
formation. Nevertheless, the topic is highly interest-
ing and deserving of much greater attention, be-
cause an understanding of this phenomenon is likely
to provide a wealth of information about the life-
history and behavior of these animals.
Not all Miocene apes were characterized by ex-
treme dimorphism. Dendropithecus, though dimor-
phic, was characterized by large canine teeth in both
48 YEARBOOK OF PHYSICAL ANTHROPOLOGY
males and females, suggesting a hylobatid-like mat-
ing system, or at least high-intensity intrasexual
competition in both males and females (Fleagle,
1999). Afropithecus canine dimorphism appears to
be reduced through specialization of male and fe-
male canines for opening hard fruit, analogous to
modern pithecines (Leakey and Walker, 1997). Re-
cently, Alba et al. (2001) suggested that canine re-
duction in Oreopithecus indicates the evolution of
chimpanzee-like mating systems, or at least sug-
gests a reduction in levels of male-male competition.
They also suggested that the pattern of canine and
dental reduction in Oreopithecus indicates overall
neoteny throughout the dentition of these animals.
Bonis and Koufos (2001) suggested that canine re-
duction in Ouranopithecus is a shared derived fea-
ture with hominids. However, Kelley (2001) demon-
strated that male canines in Ouranopithecus are as
substantial as in any other Miocene ape.
Dimorphism in hominids
One of the key defining characters of hominids is
canine reduction (White et al., 1994; Fleagle, 1999).
Australopithecus afarensis, A. africanus, Paranthro-
pus robustus, and P. boisei show small canines by
comparison to living hominoids (Plavcan and van
Schaik, 1997a) and modest to slight canine dimor-
phism. This statement needs to be qualified. In dis-
cussing canine tooth size in hominids, it is common
to refer to the canines as large, big, or robust by
comparison to those of Homo. However, such quali-
fiers need to placed in context. Compared to Homo,
chimpanzees have large canines and substantial ca-
nine dimorphism. But compared to most other pri-
mates, chimpanzee canines are relatively small in
both males and females, and canine dimorphism is
minimal. Hence, the perspective of the viewer needs
to be specified. Using a model of living primates,
most hominids (with the possible exception of A.
anamensis) had small canines and minimal canine
dimorphism. Compared to humans, it appears that
earlier hominids had relatively large canines and
greater canine dimorphism than Homo.
Ardipithecus ramidus and Australopithecus ana-
mensis, two of the earliest known hominids to date,
are interesting because they apparently had bigger
canines than later hominids (White et al., 1994;
Leakey et al., 1995). While Ardipithecus ramidus
canines are described as smaller than those of living
chimpanzees (White et al., 1994), A. anamensis ca-
nines in particular are described by Leakey et al.
(1995) as larger than those of A. afarensis, and char-
acterized by robust roots. Apparently, there is the
potential that canine dimorphism in A. anamensis
may have been substantial. A ratio of largest to
smallest specimens published by Leakey et al.
(1995) yields a dimorphism of 41% and 28% for the
mandibular mesiodistal and buccolingual dimen-
sions, respectively. This is comparable to that seen
in Gorilla gorilla. This would be truly impressive,
and might suggest that reduced canine dimorphism
[Vol. 44, 2001
is not a feature that unites all hominids. However,
these figures need to be approached with great cau-
tion. First, sample sizes are small, meaning that
dimorphism could easily be overestimated, espe-
cially by simply estimating dimorphism as a ratio of
the largest to smallest specimens available. Second,
among primates, dimorphism of the occlusal dimen-
sions of canine teeth (as opposed to the crown height
of the tooth) is poorly correlated with behavioral
estimates of male-male competition. Plavcan and
van Schaik (1997a) argue that dimorphism of occlu-
sal dimensions is unreliable, except in extreme
cases, for inferring anything about social behavior in
primates. Nevertheless, A. anamensis is tantalizing
in that it opens up the possibility of greater variabil-
ity in canine size and dimorphism among early
hominids than has previously been suspected.
Ardipithecus ramidus has been claimed to lie at
the base of the hominid radiation (White et al.,
1994). If the common ancestor of chimpanzees and
humans predates Ardipithecus by a relatively short
time, this suggests either that canine reduction hap-
pened rapidly in the earliest hominids, or that large
canine size reevolved in chimpanzees. The former
hypothesis seems the more likely, though of course
only more data from the fossil record can give us a
reliable picture of the evolution of canine dimor-
phism at this time.
In contrast to the canine teeth, dimorphism in
hominid body mass was apparently quite substan-
tial. McHenry (1992, 1994a,b) provides data sug-
gesting that body mass dimorphism in early homin-
ids ranged from comparable to a chimpanzee in
Australopithecus robustus, to quite gorilla-like in A.
boisei (Plavcan and van Schaik, 1997a). Interest-
ingly, the data of McHenry (1992, 1994a,b) suggest
that Homo erectus, considered as a single species,
could have shown substantial body size dimorphism.
However, if traditional H. erectus is split into H.
erectus sensu stricto and H. ergaster, then the levels
of dimorphism are reduced to levels more compara-
ble to modern humans. Regardless, analyses of the
face and skeletal elements of early hominids all sug-
gest that body mass dimorphism in these animals
was substantial (e.g., Leutenegger and Shell, 1987;
Hartwig-Scherer, 1993; Richmond and Jungers,
1995; Lockwood et al., 1996; Aiello and Wood, 1994;
Lockwood, 1999).
Sexual dimorphism has long been used as evi-
dence of either monogamy or polygyny in hominids
(Lovejoy, 1981; Foley and Lee, 1989; McHenry,
1994a,b; Plavcan and van Schaik, 1997a). The prob-
lem with using dimorphism to infer behavior in
early hominids is the unique combination of mini-
mal canine size dimorphism and intense body mass
dimorphism (Plavcan and van Schaik, 1997a). While
this pattern of dimorphism is shared with living
great apes (Leutenegger and Shell, 1987), the mag-
nitude of the differences is unique (Plavcan and van
Schaik, 1997a). In terms of current comparative
models for the evolution of canine and body mass
J.M. Plavcan] DIMORPHISM IN PRIMATES
dimorphism in primates, there is no clear explana-
tion for the hominid pattern. Small canines and
canine dimorphism imply a lack of male-male com-
petition, while the strong body mass dimorphism is
consistent with intense male-male competition
(Plavcan and van Schaik, 1997a). Greenfield (1992a)
provides a detailed evaluation of theories for canine
reduction in hominids, and concludes that none suf-
ficiently explains the phenomenon. The most popu-
lar explanation is that hand-held weapons sup-
planted the use of the canine teeth in male-male
competition (Brace, 1972). However, canine reduc-
tion predates the appearance of tools in the fossil
record by millions of years, and fails to explain why
canines would still not be useful (Plavcan and van
Schaik, 1997a). It could be that large male size is
maintained for some other reason apart from sexual
selection, that female choice favored large males,
that large male size is retained in early hominids
through a time lag in its response to a relaxation of
the selection for large male size, or that there was
selection for early maturation in females. None of
these hypotheses can readily be tested with current
data from the fossil record. The important point is
that the pattern of dimorphism is unique, and that
there are a number of reasonable hypotheses to ex-
plain it (Plavcan and van Schaik, 1997a), none of
which can be certainly excluded. Hence, while our
understanding of the evolution of dimorphism in
primates has increased dramatically, the evolution
of dimorphism in our own lineage remains an in-
triguing puzzle.
CONCLUSIONS
This essay provides a brief survey of sexual dimor-
phism in primates: its expression, the causes of its
evolution, and a brief documentation of its presence
in the fossil record. Sexual dimorphism as a phe-
nomenon is widely familiar. There is even today a
strong tendency to view dimorphism as a unitary
character that evolves as a simple consequence of
sexual selection. Hopefully this survey has given the
reader a sense of the complexity of the phenomenon.
There is wide variation in the expression of sexual
dimorphism among primates, both in its magnitude
and in its pattern. Underlying this variety is a pleth-
ora of mechanisms that cause or influence the ex-
pression and evolution of sexual dimorphism. There
is a rich history of comparative studies of sexual
dimorphism, through which ideas have slowly
changed as students of the topic have realized the
subtle difficulties associated with testing the sexual
selection hypothesis. There has been enormous
progress in understanding that sexual dimorphism
is a function of selective pressures on both male and
female traits, and that a complete model of the evo-
lution of dimorphism must describe the mechanisms
affecting both males and females. It is now apparent
that sexual selection, mating systems, and esti-
mates of the frequency and intensity of male-male
competition do not measure the same thing. This
49
leads us to the conclusion that sexual dimorphism is
not a simple function of differential male reproduc-
tive success, but also of pressures on males for dis-
play, of the interaction between the utility of differ-
ent traits as weapons and different fighting
strategies at different sizes and in different habi-
tats, and of female counterstrategies against male
domination of mating patterns. Dimorphism is also
a function of different developmental pathways, all
of which can be affected by different selective pres-
sures throughout an animals entire life-history. Un-
derstanding these pathways and the selective forces
that mold them gives profound insights into the
evolution of dimorphism. Finally, the fossil record
teaches us that our extant models do not embrace
the full range of the expression of sexual dimor-
phism in primates. Models based on living species
must pass the test of being able to explain the full
range of dimorphism in all primates, including those
from the past.
In spite of all this, there are still very large gaps in
our understanding of the evolution of sexual dimor-
phism. Comparative behavioral-ecological models
are far from perfect, and are in constant need of
updating. Comparative paternity data alone would
be immensely valuable in identifying and testing
different models of the selective basis for dimor-
phism in primates. Current genetic techniques have
finally made this possible, but as of yet we have no
comparative database adequate to this task. Studies
on the ontogeny of dimorphism have only just begun.
Broadly based comparative patterns of dimorphism
are only now being carefully documented and scru-
tinized. Models of functional and biomechanical con-
straints that could give rise to different patterns of
dimorphism have not been adequately explored.
Hopefully, the future will see an increasing recogni-
tion of the wealth of information on primate evolu-
tion that can be gleaned from understanding sexual
dimorphism.
ACKNOWLEDGMENTS
I thank the many people who have discussed this
topic with me (and critically reviewed my papers)
over the years, especially Rich Kay, Carel van
Schaik, Steve Leigh, Tom Masterson, Mike Lague,
Charlie Nunn, Jay Kelley, Peter Kappeler, Sue
Ford, Bernard Wood, Bill Kimbel, Dana Cope, Patri-
cia Vinyard, Gene Albrecht, Rebecca German, Ken
Glander, John Fleagle, Elwyn Simons, Charlie Lock-
wood, Callum Ross, Bill Jungers, Scott McGraw,
Mike Peirera, Pat Wright, Matt Cartmill, Matt Ra-
vosa, Greg Gunnell, Phil Gingerich, Walter Leu-
tenegger, Paul OHiggins, and Richard Smith. I also
thank the many curators and their staffs at muse-
ums throughout the US, Europe, and South Africa
who have been so generous over the years in helping
me study the material in their care. Kamla Ahluwa-
lia kindly reviewed a draft of this manuscript. I
thank Chris Ruff and two anonymous reviewers for
thoughtful comments that greatly improved the
50 YEARBOOK OF PHYSICAL ANTHROPOLOGY
manuscript. Chris Ruff is a very patient editor. This
paper was partly supported by NSF SBR 9616671.
LITERATURE CITED
Aiello LC, Wood BA. 1994. Cranial variables as predictors of
hominine body mass. Am J Phys Anthropol 95:409 426.
Alba DM, Moya-Sola S, Kohler M. 2001. Canine reduction in the
Miocene hominoid Oreopithecus bambolii: behavioural and evo-
lutionary implications. J Hum Evol 40:116.
Anderson RW Jr. 1981. Sexual dimorphism in the cranium of
Cercopithecus aethiops. J Hum Evol 10:311317.
Anderson RW Jr. 1982. Sexual dimorphism in the cranium of
Cercocebus albigena. J Hum Evol 10:143150.
Andersson M. 1994. Sexual selection. Princeton: Princeton Uni-
versity Press.
Bonis L, Koufos GD. 2001. Phylogenetic relationships of Ouran-
opithecus macedoniensis (Mammalia, Primates, Hominoidea,
Hominidae) of the late Miocene deposits of Central Macedonia
(Greece). In: Bonis L, Koufos GD, Andrews P, editors. Phylog-
eny of the neogene hominoid primates of Eurasia. Cambridge,
UK: Cambridge University Press. p 254 268.
Brace CL. 1972. Sexual dimorphism in human evolution. Yrbk
Phys Anthropol 16:31 49.
Brennan EJ. 1985. De Brazzas monkeys (Cercopithecus neglec-
tus) in Kenya: census, distribution and conservation. Am J
Primatol 8:269 277.
Cheverud JM, Dow MM, Leutenegger W. 1985. The quantitative
assessment of phylogenetic constraints in comparative analy-
sis: sexual dimorphism in body weight among primates. Evo-
lution 38:13351351.
Clutton-Brock TH. 1985. Size, sexual dimorphism, and polygyny
in primates. In: Jungers WL, editor. Size and scaling in primate
biology. New York: Plenum Press. p 51 60.
Clutton-Brock TH, Harvey PH, Rudder B. 1977. Sexual dimor-
phism, socionomic sex ratio and body weight in primates. Na-
ture 269:191195.
Cochard LR. 1985. Ontogenetic allometry of the skull and denti-
tion of the rhesus monkey (Macaca mulatta). In: Jungers WL,
editor. Size and scaling in primate biology. New York: Plenum
Press. p 231256.
Cole TM, Smith FH. 1987. An odontometric assessment of vari-
ability in Australopithecus afarensis. J Hum Evol 3:221234.
Cope DA. 1993. Measures of variation as indicators of multiple
taxa in samples of sympatric Cercopithecus species. In: Kimbel
WH, Martin LB, editors. Species, species concepts, and primate
evolution. New York: Plenum Press. p 211237.
Cope DA, Lacy MG. 1992. Falsification of a single species hypoth-
esis using the coefficient of variation: a simulation approach.
Am J Phys Anthropol 89:359 378.
Cope DA, Lacy MG. 1994. Testing single species hypotheses using
the combined referent CV: applications to fossil hominoid den-
tal samples. Am J Phys Anthropol [Suppl] 16:71.
Corner BD, Richtsmeier JT. 1991. Morphometric analysis of
craniofacial growth in Cebus apella. Am J Phys Anthropol
84:323342.
Corner BD, Richtsmeier JT. 1992. Cranial growth in the squirrel
monkey (Saimiri sciureus): a quantitative analysis using three-
dimensional coordinate data. Am J Phys Anthropol 87:67 82.
Corner BD, Richtsmeier JT. 1993. Cranial growth and growth
dimorphism in Ateles geoffroyi. Am J Phys Anthropol 92:371
394.
Covert HH, Williams BA. 1994. Recent recovered specimens of
North American Eocene omomyids and adapids and their bear-
ing on debates about anthropoid origins. In: Fleagle JG, Kay
RF, editors. Anthropoid origins. New York: Plenum Press. p
29 54.
Crook JH. 1972. Sexual selection, dimorphism, and social orga-
nization in the primates. In: Campbell B, editor. Sexual selec-
tion and the descent of man 18711971. Chicago: Aldine. p
231281.
Darwin C. 1871. The descent of man, and selection in relation to
sex. London: J. Murray.
[Vol. 44, 2001
Demment MW. 1983. Feeding ecology and the evolution of body
size in baboons. Afr J Ecol 21:219 233.
DeVore I, Washburn SL. 1963. Baboon ecology and human evo-
lution. In: Howell FC, Bourliere F, editors. African ecology and
human evolution. Chicago: Aldine. p 335367.
Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, van den
Bussche R. 2001. Major-histocompatibility-complex-associated
variation in secondary sexual traits of white-tailed deer
(Odocoileus virginianus): evidence for good-genes advertise-
ment. Evolution 55:616 625.
Dixson AF. 1987. Observations of the evolution of the genitalia
and copulatory behaviour in male primates. J Zool Lond 213:
423 443.
Dixson AF. 1997. Sexual selection and evolution of the seminal
vesicles in primates. Folia Primatol (Basel) 69:300 306.
Ely J, Kurland JA. 1989. Spatial autocorrelation, phylogenetic
constraints, and the causes of sexual dimorphism in primates.
Int J Primatol 10:151171.
Emlen ST, Oring T. 1977. Ecology, sexual selection, and the
evolution of mating systems. Science 191:215233.
Fairbairn DJ. 1897. Allometry for sexual size dimorphism: pat-
tern and process in the coevolution of body size in males and
females. Annu Rev Ecol Syst 28:659 687.
Fedigan L, Fedigan LM. 1988. Cercopithecus aethiops: a review of
field studies. In: Gautier-Hion A, Bourliere F, Gautier JP, ed-
itors. A primate radiation: evolutionary biology of the African
guenons. Cambridge: Cambridge University Press. p 389 411.
Fisher RA. 1930. The genetical theory of natural selection. Ox-
ford: Clarendon.
Fleagle JG. 1999. Primate adaptation and evolution, 2nd ed. New
York: Academic Press.
Fleagle JG, Kay RF, Simons EL. 1980. Sexual dimorphism in
early anthropoids. Nature 287:328 330.
Foley RA, Lee PC. 1989. Finite social space, evolutionary path-
ways, and reconstructing hominid behavior. Science 243:901
906.
Fooden J. 1980. Classification and distribution of living macaques
(Macaca Lacepede 1799). In: Lindburg DG, editor. The ma-
caques: studies in ecology, behavior, and evolution. New York:
Van Nostrand Reinhold Co. p 19.
Ford SM. 1994. Evolution of sexual dimorphism in body weight in
platyrrhines. Am J Primatol 34:221224.
Frayer DW. 1980. Sexual dimorphism and cultural evolution in
the late Pleistocene and Holocene of Europe. J Hum Evol
9:399 415.
Garn SM, Kerewsky RS, Swindler DR. 1966. Canine field in
sexual dimorphism of tooth size. Nature 212:15011502.
Gaulin SJC, Sailer LD. 1984. Sexual dimorphism in weight
among primates: the relative impact of allometry and sexual
selection. Int J Primatol 5:515535.
Gautier-Hion A, Gautier JP. 1985. Sexual dimorphism, social
units and ecology among sympatric forest guenons. In: Gues-
quiere J, Martin RD, Newcombe F, editors. Human sexual
dimorphism. London: Taylor and Francis. p 6177.
Gingerich PD. 1981. Cranial morphology and adaptations in Eo-
cene Adapidae. I. Sexual dimorphism in Adapis magnus and
Adapis parisiensis. Am J Phys Anthropol 56:217234.
Gingerich PD. 1995. Sexual dimorphism in earliest Eocene Can-
tius torresi (Mammalia, Primates, Adapoidea). Contrib Mus
Paleontol Univ Mich 29:185199.
Gingerich PD, Schoeninger MJ. 1979. Patterns of tooth size vari-
ability in the dentition of primates. Am J Phys Anthropol
51:457 466.
Godfrey LR, Lyon SK, Sutherland MR. 1993. Sexual dimorphism
in large-bodied primates: the case of the subfossil lemurs. Am J
Phys Anthropol 90:315334.
Greenfield LO. 1992a. Origin of the human canine: a new solution
to an old enigma. Yrbk Phys Anthropol 35:153185.
Greenfield LO. 1992b. Relative canine size, behavior, and diet in
male ceboids. J Hum Evol 23:469 480.
Greenfield LO. 1996. Correlated response of homologous charac-
teristics in the anthropoid anterior dentition. J Hum Evol 31:
119.
J.M. Plavcan] DIMORPHISM IN PRIMATES
Greenfield LO. 1998. Canine tip wear in male and female anthro-
poids. Am J Phys Anthropol 107:8796.
Greenfield LO, Washburn A. 1991. Polymorphic aspects of male
anthropoid canines. Am J Phys Anthropol 84:1734.
Greenfield LO, Washburn A. 1992. Polymorphic aspects of male
anthropoid honing premolars. Am J Phys Anthropol 87:173
186.
Gustafsson JA. 1994. Regulation of sexual dimorphism in rat
liver. In: Short RV, Balaban E, editors. The differences between
the sexes. Cambridge: Cambridge University Press. p 231241.
Harcourt AH. 1995. Sexual selection and sperm competition in
primates: what are male genitalia good for? Evol Anthropol
4:121129.
Harcourt AH, Gardiner J. 1994. Sexual selection and genital
anatomy of male primates. Proc R Soc Lond [Biol] 255:4753.
Hartwig-Scherer S. 1993. Body weight prediction in early homi-
nids: towards a taxon-independent approach. Am J Phys An-
thropol 92:1736.
Harvey PH, Kavanagh M, Clutton-Brock TH. 1978. Sexual dimor-
phism in primate teeth. J Zool Lond 186:474 485.
Hayes VJ, Freedman L, Oxnard CE. 1995. The differential ex-
pression of dental sexual dimorphism in subspecies of Colobus
guereza. Int J Primatol 16:971996.
Hershkovitz P. 1977. Living New World monkeys (Platyrrhini).
Volume 1. Chicago: University of Chicago Press.
Jacobs GH. 1994. Variations in primate color vision: mechanisms
and utility. Evol Anthropol 3:196 205.
Janson CH, van Schaik CP. 1993. Ecological risk aversion in
juvenile primates: slow and steady wins the race. In: Pereira
ME, Fairbanks LA, editors. Juvenile primates. New York: Ox-
ford University Press. p 5774.
Jones AL, Degusta D, Turner SP, Campbell J, Milton K. 2000.
Craniometric variation in a population of mantled howler mon-
keys (Alouatta palliata): evidence of size selection in females
and growth in dentally mature males. Am J Phys Anthropol
113:411 434.
Kappeler PM. 1990. The evolution of sexual size dimorphism in
prosimian primates. Am J Primatol 21:201214.
Kappeler PM. 1991. Patterns of sexual dimorphism in body
weight among prosimian primates. Folia Primatol (Basel) 57:
132146.
Kappeler PM. 1996. Intrasexual selection and phylogenetic con-
straints in the evolution of sexual canine dimorphism in strep-
sirrhine primates. J Evol Biol 9:43 65.
Kappeler PM. 1999. Primate socioecology: new insights from
males. Naturwissenschaften 85:18 29.
Kay RF, Plavcan JM, Glander KE, Wright PC. 1988. Sexual
selection and canine dimorphism in New World monkeys. Am J
Phys Anthropol 77:385397.
Kelley J. 1986. Species recognition and sexual dimorphism in
Proconsul and Rangwapithecus. J Hum Evol 15:461 495.
Kelley J. 1989. Behavioral implications of sexual dimorphism in
Australopithecus afarensis. Am J Phys Anthropol 78:251.
Kelley J. 1993. Taxonomic implications of sexual dimorphism in
Lufengpithecus. In: Kimbel WH, Martin LB, editors. Species,
species concepts, and primate evolution. New York: Plenum
Press. p 429 458.
Kelley J. 1995a. Sex determination in Miocene catarrhine pri-
mates. Am J Phys Anthropol 96:391 417.
Kelley J. 1995b. Sexual dimorphism in canine shape among ex-
tant great apes. Am J Phys Anthropol 96:365389.
Kelley J. 2001. Phylogeny and sexually dimorphic characters:
canine reduction in Ouranopithecus. In: Bonis L, Koufos GD,
Andrews P, editors. Phylogeny of the neogene hominoid pri-
mates of Eurasia. Cambridge: Cambridge University Press. p
269 283.
Kelley J, Etler D. 1989. Hominoid dental variability and species
number at the late Miocene site of Lufeng, China. Am J Pri-
matol 18:1534.
Kelley J, Plavcan JM. 1998. A simulation test of hominoid species
number at Lufeng, China: implications for the use of the coef-
ficient of variation in paleotaxonomy. J Hum Evol 35:577596.
Kelley J, Xu Q. 1991. Extreme sexual dimorphism in a Miocene
hominoid. Nature 352:151153.
51
Kimbel WL, White TD. 1988. Variation, sexual dimorphism and
the taxonomy of Australopithecus. In: Grine FE, editor. Evolu-
tionary history of the robust australopithecines. New York:
Aldine de Gruyter. p 175192.
Kinzey WG. 1992. Dietary and dental adaptations in the Pithe-
ciinae. Am J Phys Anthropol 88:499 514.
Kramer A, Donnelly SM, Kidder JH, Ousley SD, Olah SM. 1995.
Craniometric variation in large-bodied hominoids: testing the
single-species hypothesis for Homo habilis. J Hum Evol 29:
443 462.
Krishtalka L, Stucky RK, Beard KC. 1991. The earliest fossil
evidence for sexual dimorphism in primates. Proc Natl Acad Sci
USA 87:52235226.
Lague MR. 2000. Patterns of sexual dimorphism in the joint
surfaces of the elbow and knee of catarrhine primates. Ph.D.
dissertation, State University of New York at Stony Brook.
Lande R. 1980. Sexual dimorphism, sexual selection, and adap-
tation in polygenic characters. Evolution 33:292305.
Leakey M, Walker A. 1997. Afropithecus function and phylogeny.
In: Begun DR, Ward CV, Rose MD, editors. Function, phylog-
eny, and fossils: Miocene hominoid evolution and adaptations.
New York: Plenum. p 225239.
Leakey MG, Feibel CS, McDougall I, Walker A. 1995. New four-
million-year-old hominid species from Kanapoi and Allia Bay,
Kenya. Nature 376:565571.
Le Gros Clark WE. 1971. The antecedents of man. New York:
Quadrangle Books.
Leigh SR. 1992. Patterns of variation in the ontogeny of primate
body size dimorphism. J Hum Evol 23:2750.
Leigh SR. 1995a. Ontogeny and the evolution of body size dimor-
phism in primates. Anthropologie 33:1728.
Leigh SR. 1995b. Socioecology and the ontogeny of sexual size
dimorphism in anthropoid primates. Am J Phys Anthropol
97:339 356.
Leigh SR, Cheverud JM. 1991. Sexual dimorphism in the baboon
facial skull. Am J Phys Anthropol 84:193208.
Leigh SR, Shea BT. 1995. Ontogeny and the evolution of adult
body size dimorphism in apes. Am J Primatol 36:37 60.
Leigh SR, Terranova CJ. 1998. Comparative perspectives on bi-
maturism, ontogeny, and dimorphism in lemurid primates. Int
J Primatol 19:723749.
Leutenegger W, Cheverud JM. 1982. Correlates of sexual dimor-
phism in primates: ecological and size variables. Int J Primatol
3:387 402.
Leutenegger W, Cheverud JM. 1985. Sexual dimorphism in pri-
mates: the effects of size. In: Jungers WL, editor. Size and
scaling in primate biology. New York: Plenum Press. p 3350.
Leutenegger W, Kelly JT. 1977. Relationship of sexual dimor-
phism in canine size and body size to social, behavioral and
ecological correlates in anthropoid primates. Primates 18:117
136.
Leutenegger W, Larson S. 1985. Sexual dimorphism in the post-
cranial skeleton of New World primates. Folia Primatol (Basel)
44:8295.
Leutenegger W, Lubach G. 1987. Sexual dimorphism, mating
system, and the effect of phylogeny in De Brazzas monkey
(Cercopithecus neglectus). Am J Primatol 13:171179.
Leutenegger W, Masterson TJ. 1989a. The ontogeny of sexual
dimorphism in the cranium of Bornean orang-utans (Pongo
pygmaeus pygmaeus): I. Univariate analysis. Z Morphol An-
thropol 78:114.
Leutenegger W, Masterson TJ. 1989b. The ontogeny of sexual
dimorphism in the cranium of Bornean orang-utans (Pongo
pygmaeus pygmaeus): II. Allometry and heterochrony. Z Mor-
phol Anthropol 78:1524.
Leutenegger W, Shell B. 1987. Variability and sexual dimorphism
in canine size in Australopithecus and extant hominoids. J
Hum Evol 16:359 367.
Lieberman SS, Gelvin BR, Oxnard CE. 1985. Dental sexual di-
morphisms in some extant hominoids and ramapithecines from
China: a quantitative approach. Am J Primatol 9:305326.
Lindenfors P, Tullberg BS. 1998. Phylogenetic analysis of pri-
mate size evolution: the consequences of sexual selection. Biol J
Linn Soc 64:413 447.
52 YEARBOOK OF PHYSICAL ANTHROPOLOGY
Lockwood CA. 1999. Sexual dimorphism in the face of Australo-
pithecus africanus. J Hum Evol 31:537548.
Lockwood CA, Richmond BG, Jungers WL, Kimbel WH. 1996.
Randomization procedures and sexual dimorphism in Austra-
lopithecus afarensis. J Hum Evol 31:537548.
Lovejoy CO. 1981. The origin of man. Science 211:341350.
Lucas PW. 1981. An analysis of canine size and jaw shape in some
Old and New World non-human primates. J Zool Lond 195:
437 448.
Lucas PW, Corlett RT, Luke DA. 1986. Sexual dimorphism in
tooth size in anthropoids. Hum Evol 1:2339.
Martin L. 1991. Teeth, sex, and species. Nature 352:111112.
Martin RD, Willner LA, Dettling A. 1994. The evolution of sexual
size dimorphism in primates. In: Short RV, Balaban E, editors.
The differences between the sexes. Cambridge: Cambridge Uni-
versity Press. p 159 200.
Masterson TJ. 1997. Sexual dimorphism and interspecific cranial
form in two capuchin species: Cebus albifrons and C. apella.
Am J Phys Anthropol 104:487512.
Masterson TJ, Hartwig WC. 1998. Degrees of sexual dimorphism
in Cebus and other New World monkeys. Am J Phys Anthropol
107:243256.
Masterson TJ, Leutenegger W. 1990. The ontogeny of sexual
dimorphism in the cranium of Bornean orang-utans (Pongo
pygmaeus pygmaeus) as detected by principal-components
analysis. Int J Primatol 11:517539.
McHenry HM. 1992. Body size and proportions in early hominids.
Am J Phys Anthropol 87:407 431.
McHenry HM. 1994a. Behavioral ecological implications of early
hominid body size. J Hum Evol 27:77 87.
McHenry HM. 1994b. Sexual dimorphism in fossil hominids and
its sociological implications. In: Shennan S, Steele J, editors.
Power, sex and tradiation: the archeology of human ancestry.
London: Routledge and Kegan Paul. p 91109.
Miller JMA. 1991. Does brain size variability provide evidence of
multiple species in Homo habilis? Am J Phys Anthropol 84:
385398.
Miller JMA. 2000. Craniofacial variation in Homo habilis: an
analysis of the evidence for multiple species. Am J Phys An-
thropol 112:103128.
Milton K. 1985. Multimale mating and the absence of canine
tooth dimorphism in woolly spider monkeys (Brachyteles arach-
noides). Am J Phys Anthropol 68:519 523.
Mitani J, Gros-Louis J, Richards AF. 1996. Sexual dimorphism,
the operational sex ratio, and the intensity of male competition
in polygynous primates. Am Nat 147:966 980.
Napier PH. 1981. Catalogue of primates in the British Museum
(Natural History) and elsewhere in the British Isles. Part II:
family Cercopithecidae, subfamily Cercopithecinae. London:
British Museum (Natural History).
Napier PH. 1985. Catalogue of primates in the British Museum
(Natural History) and elsewhere in the British Isles. Part III:
family Cercopithecidae, subfamily Colobinae. London: British
Museum (Natural History).
Nunn CL. 1999. The evolution of exaggerated sexual swellings in
primates and the graded-signal hypothesis. Anim Behav 58:
229 246.
OHiggins PO, Moore WJ, Johnson DR, McAndrew TJ. 1990.
Patterns of cranial sexual dimorphism in certain groups of
extant hominoids. J Zool Lond 222:399 420.
Oxnard CE. 1987. Fossils, teeth and sex: new perspectives on
human evolution. Seattle: University of Washington Press.
Pagel M. 1994. The evolution of conspicuous oestrus advertise-
ment in Old World monkeys. Anim Behav 47:13331341.
Phillips-Conroy JE, Jolly CJ. 1981. Sexual dimorphism in two
subspecies of Ethiopian baboons (Papio hamadryas) and their
hybrids. Am J Phys Anthropol 56:115129.
Pickford M. 1986. On the origins of body size dimorphism in
primates. In: Pickford M, Chiarelli B, editors. Sexual dimor-
phism in living and fossil primates. Florence: Il Sedicesimo. p
7791.
Plavcan JM. 1990. Sexual dimorphism in the dentition of extant
anthropoid primates. Ph.D. dissertation. Ann Arbor: Univer-
sity Microfilms.
[Vol. 44, 2001
Plavcan JM. 1993a. Canine size and shape in male anthropoid
primates. Am J Phys Anthropol 92:201216.
Plavcan JM. 1993b. Catarrhine dental variability and species
recognition in fossils. In: Kimbel WH, Martin LB, editors. Spe-
cies, species concepts, and primate evolution. New York: Ple-
num Press. p 239 263.
Plavcan JM. 1998. Correlated response, competition, and female
canine size in primates. Am J Phys Anthropol 107:401 416.
Plavcan JM. 1999. Mating systems, intrasexual competition and
sexual dimorphism in primates. In: Lee PC, editor. Compara-
tive primate socioecology. Cambridge: Cambridge University
Press. p 241269.
Plavcan JM. 2000a. Inferring social behavior from sexual dimor-
phism in the fossil record. J Hum Evol 39:327344.
Plavcan JM. 2000b. Variance dimorphism in primates. Am J Phys
Anthropol [Suppl] 30:251.
Plavcan JM. n.d. Taxonomic variation in the patterns of cranio-
facial dimorphism in primates. J Hum Evol (in press).
Plavcan JM, Cope DA. 2001. Metric variation and species recog-
nition in the fossil record. Evol Anthropol (in press).
Plavcan JM, Kay RF. 1988. Sexual dimorphism and dental vari-
ability in platyrrhine primates. Int J Primatol 9:169 178.
Plavcan JM, Kelley J. 1996. Evaluating the dual selection hy-
pothesis of canine reduction. Am J Phys Anthropol 99:379 387.
Plavcan JM, van Schaik CP. 1992. Intrasexual competition and
canine dimorphism in anthropoid primates. Am J Phys An-
thropol 87:461 477.
Plavcan JM, van Schaik CP. 1994. Canine dimorphism. Evol
Anthropol 2:208 214.
Plavcan JM, van Schaik CP. 1997a. Interpreting hominid behav-
ior on the basis of sexual dimorphism. J Hum Evol 32:345374.
Plavcan JM, van Schaik CP. 1997b. Intrasexual competition and
body weight dimorphism in anthropoid primates. Am J Phys
Anthropol 103:37 68.
Plavcan JM, van Schaik CP, Kappeler PM. 1995. Competition,
coalitions and canine size in primates. J Hum Evol 28:245276.
Pope TR. 2000. Reproductive success increases with degree of
kinship in cooperative coalitions of female red howler monkeys
(Alouatta seniculus). Behav Ecol Sociobiol 48:253267.
Ravosa MJ. 1990. Functional assessment of subfamily variation
in maxillomandibular morphology among Old World monkeys.
Am J Phys Anthropol 82:199 212.
Ravosa MJ. 1991. The ontogeny of cranial sexual dimorphism in
two Old World monkeys: Macaca fascicularis (Cercopithecinae)
and Nasalis larvatus (Colobinae). Int J Primatol 12:403 426.
Ravosa MJ, Ross CF. 1994. Craniodental allometry and hetero-
chrony in two howler monkeys: Alouatta seniculus and A. pal-
liata. Am J Primatol 33:277299.
Reiss MJ. 1986. Sexual dimorphism in body size: are larger spe-
cies more dimorphic? J Theor Biol 121:163172.
Rensch B. 1960. Evolution above the species level. New York:
Columbia University Press.
Reynolds JD, Harvey PH. 1994. Sexual selection and the evolu-
tion of sex differences. In: Short RV, Balaban E, editors. The
differences between the sexes. Cambridge: Cambridge Univer-
sity Press. p 5370.
Richmond BG, Jungers WL. 1995. Size variation and sexual di-
morphism in Australopithecus afarensis and living hominoids.
J Hum Evol 29:229 245.
Richtsmeier JT, Cheverud JM. 1989. Sexual dimorphism of facial
growth in Macaca mulatta and M. fascicularis. Fortschr Zool
35:438 440.
Richtsmeier JT, Cheverud JM, Danahey SE, Corner BD, Lele S.
1993. Sexual dimorphism of ontogeny in the crab-eating ma-
caque (Macaca fascicularis). J Hum Evol 25:130.
Ross C, Williams B, Kay RF. 1998. Phylogenetic analysis of an-
thropoid relationships. J Hum Evol 35:221306.
Rowell TE, Chism J. 1986. Sexual dimorphism and mating sys-
tems: jumping to conclusions. In: Pickford M, Chiarelli B, edi-
tors. Sexual dimorphism in living and fossil primates. Florence:
Il Sedicesimo. p 107111.
Ryan MJ. 1990. Sexual selection, sensory systems and sensory
exploitation. Oxf Surv Evol Biol 7:157195.
J.M. Plavcan] DIMORPHISM IN PRIMATES
Schwartz GT, Dean MC. 2001. The ontogeny of canine dimor-
phism in extant hominoids. Am J Phys Anthropol 115:269 283.
Setchell JM, Dixson AF. 2001. Circannual changes in the second-
ary sexual adornments of semifree-ranging male and female
mandrills (Mandrillus sphinx). Am J Primatol 53:109 121.
Shea BT. 1986. Ontogenetic approaches to sexual dimorphism in
anthropoids. J Hum Evol 1:97110.
Simons EL, Plavcan JM, Fleagle JG. 1999. Canine sexual dimor-
phism in Egyptian Eocene anthropoid primates: Catopithecus
and Proteopithecus. Proc Natl Acad Sci USA 96:2559 2562.
Small MF. 1989. Female choice in nonhuman primates. Yrbk
Phys Anthropol 32:103127.
Smith RJ, Jungers WL. 1997. Body mass in comparative prima-
tology. J Hum Evol 32:523559.
Smuts BB, Smuts RW. 1993. Male aggression and sexual coercion
of females in nonhuman primates and other mammals: evi-
dence and theoretical implications. Adv St Behav 22:1 63.
Spencer MA, Hogard R. 2001. Biomechanics of sexual dimor-
phism in the anthropoid masticatory system. Am J Phys An-
thropol [Suppl] 32:141.
Stallmann RR, Froehlich JW. 2000. Primate sexual swellings as
coevolved signal systems. Primates 41:116.
Stammbach E. 1987. Desert, forest and montane baboons: multi-
level societies. In: Smuts BB, Cheney DL, Seyfarth RM, Wrang-
ham RW, Struhsaker TT, editors. Primate societies. Chicago:
University of Chicago Press. p 112120.
Sterk EHM. 1997. Determinants of female dispersal in Thomas
langurs. Am J Primatol 42:1789 198.
Stern JT, Susman RL. 1983. The locomotor anatomy of Austra-
lopithecus afarensis. Am J Phys Anthropol 60:279 317.
Trivers RL. 1972. Parental investment and sexual selection. In:
Campbell B, editor. Sexual selection and the descent of man
18711971. Chicago: Aldine Publishing Co. p 136 179.
Turner TR, Anapol F, Jolly CJ. 1994. Body weights of adult vervet
monkeys (Cercopithecus aethiops) at four sites in Kenya. Folia
Primatol (Basel) 63:177179.
Turner TR, Anapol F, Jolly CJ. 1997. Growth, development, and
sexual dimorphism in vervet monkeys (Cercopithecus aethiops)
at four sites in Kenya. Am J Phys Anthropol 103:19 35.
53
van Schaik CP, van Noordwijk MA, Nunn CL. 1999. Sex and
social evolution in primates. In: Lee PC, editor. Comparative
primate socioecology. Cambridge: Cambridge University Press.
p 204 240.
Verrell PA. 1992. Primate penile morphologies and social sys-
tems: further evidence for an association. Folia Primatol
(Basel) 59:114 120.
Watanabe K. 1981. Variation in group composition and popula-
tion density of the two sympatric Mentawian leaf-monkeys.
Primates 22:145160.
White TD, Folkens PA. 1991. Human osteology. New York: Aca-
demic Press.
White TD, Suwa G, Asfaw B. 1994. Australopithecus ramidus, a
new species of early hominid from Aramis, Ethiopia. Nature
371:306 312.
Wolpoff MH. 1976. Some aspects of the evolution of early hominid
sexual dimorphism. Curr Anthropol 17:579 606.
Wood BA. 1976. The nature and basis of sexual dimorphism in the
primate skeleton. J Zool Lond 180:1534.
Wood B. 1993. Early Homo: how many species? In: Kimbel WH,
Martin LB, editors. Species, species concepts, and primate evo-
lution. New York: Plenum. p 485522.
Wood BA, Xu Q. 1991. Variation in the Lufeng dental remains. J
Hum Evol 20:291311.
Wood BA, Li Y, Willoughby C. 1991. Intraspecific variation and
sexual dimorphism in cranial and dental variables among
higher primates and their bearing on the hominid fossil record.
J Anat 174:185205.
Wu R. 1987. A revision of the classification of the Lufeng great
apes. Acta Anthropol Sin 6:265271.
Wu R, Oxnard CE. 1983a. Ramapithecines from China: evidence
from tooth dimensions. Nature 306:258 260.
Wu R, Oxnard CE. 1983b. Ramapithecus and Sivapithecus from
China: some implications from higher primate evolution. Am J
Primatol 5:303344.
Zihlman AL. 1985. Australopithecus afarensis: two sexes or two
species? In: Tobias PV, editor. Hominid evolution: past,
present, and future. New York: Alan R Liss. p 213220.
Zingeser MR. 1969. Cercopithecoid canine tooth honing mecha-
nisms. Am J Phys Anthropol 31:205214.