Sexual dimorphism in non-human primates
Sexual dimorphism describes the morphological, physiological, and behavioral differences between males and females of the same species. Most primates are sexually dimorphic for different biological characteristics, such as body size, canine tooth size, craniofacial structure, skeletal dimensions, pelage color, and markings and vocalization. However, such sex differences are primarily limited to the anthropoid primates; most of the strepsirrhine primates (lemurs and lorises) and tarsiers are monomorphic.
- 1 Types
- 2 Ultimate mechanisms
- 3 See also
- 4 References
Extant primates exhibit a broad range of variation in sexual size dimorphism (SSD), or sexual divergence in body size. It ranges from species such as gibbons and strepsirrhines (including Madagascar’s lemurs) in which males and females have almost the same body sizes to species such as chimpanzees and bonobos in which males’ body sizes are larger than females’ body sizes. In extreme cases, males have body sizes that are almost twice as large as those of females, as in some species including gorillas, orangutans, mandrills, hamadryas baboons, and proboscis monkeys. Patterns of size dimorphism exhibited in primates may correspond to the intensity of competition between members of the same sex for access to mates–intrasexual competition. Some callitrichine and strepsirrhine primates are, however, characterized by the reverse dimorphism, a phenomenon in which females are larger than males. For lemurs, for example, females’ dominance over males accounts for the reverse dimorphism.
Canine sexual dimorphism is one particular type of sexual dimorphism, in which males of a species have larger canines than females. Within primates, the male and female canine tooth size varies among different taxonomic subgroups, yet canine dimorphism is most extensively found in catarrhines among haplorhine primates. For example, in many baboons and macaques, the size of male canines is more than twice as large as that of female canines. It is rare, yet females in some species are known to have larger canines than males, such as the eastern brown mouse lemur (Microcebus rufus). Sexual dimorphism in canine tooth size is relatively weak or absent in extant strepsirrhine primates. The South American titi monkeys (Callicebus moloch), for instance, do not exhibit any differences in the size of canine teeth between the sexes.
Among different types of teeth constituting the dentition of primates, canines exhibit the greatest degree of variation in tooth size, whereas incisors have less variation and cheek teeth have the least. A canine dimorphism is also more widely seen in maxillary canines than in mandibular canines.
Craniofacial sex differentiation among anthropoid primates varies in a wide range and is known to arise primarily through ontogenetic processes. Studies on hominids have shown that, in general, males tend to have a greater increase of facial volume than of neurocranial volume, a more obliquely oriented foramen magnum, and a more pronounced rearrangement of the nuchal region. The breadth, length and height of the neurocranium in adult male macaques, guenons, orangutans and gorillas are about nine percent larger than the neurocranial dimensions in adult females, whereas in spider monkeys and gibbons the sex differences is on a general average about 4 to 5 percent. In orangutans, males and females share similarities in facial dimensions and growth in terms of orbits, nasal width, and facial width. They tend to have some significant differences, however, in various facial heights (e.g., height of the anterior face, premaxilla, and nose).
Primates also exhibit sexual dimorphism in skeletal structures. In general, skeletal dimorphism in primates is primarily known as a product of body mass dimorphism. Hence, males have proportionally larger skeletons compared to females due to their larger body masses. Larger and more robust skeletal structures in males is also attributable to better developed muscle scarring, and more intense cresting of bones compared to those of females. Male gorillas, for example, possess large sagittal and nuchal crests, which correspond to their large temporalis muscles and nuchal musculature. Also, an unusual skeletal dimorphism includes enlarged, hollow hyoid bones found in males of gibbons and howler monkeys, which contribute to the resonation of their voices.
Pelage color and markings
Sex differences in pelage, such as capes of hair, beards, or crests, and skin can be found in several species among adult primates. Several species (e.g., Lemur macaco, Pithecia pithecia, Alouatta caraya) show an extensive dimorphism in pelage colors or patterning. For example, in mandrills (Mandrillus sphinx), males display extensive red and blue coloration on their face, rump and genitalia as compared to females. Male mandrills also possess a yellow beard, nuchal crest of hair, and pronounced boney paranasal ridges, all of which are absent or vestigial in females. Studies have shown that male color in mandrills serves as a badge of social status in the species.
Temporary sexual dimorphism
Some sexual dimorphic traits in primates are known to appear on a temporary basis. In squirrel monkeys (Saimiri sciureus), males can gain fat as much as 25 percent of the body mass only during the breeding season, specifically in their upper torso, arms, and shoulders. This seasonal phenomenon, known as “male fattening,” is associated with both male-male competition and female choice for larger males. Orangutan males tend to gain weight and develop large cheek flanges, when they achieve dominance over other group members.
In many adult primates, dimorphism in the vocal repertoire can appear in both call production (e.g., calls with a particular set of acoustic traits) and usage (e.g., call frequency and context-specificity) between the sexes. Sex-specific calls are commonly found in Old World monkeys, in which males produce loud calls for intergroup spacing and females produce copulation calls for sexual activity. Forest guenons also tend to display strong vocal divergences between sexes, with mostly sex-specific call types. Studies on De Brazza’s monkeys (Cercopithecus neglectus), one of the African guenon species, have shown that call rates in adult females (24 call.hr-1) are more than seven times higher than in adult males (2.5call.hr-1). A usage of different call types also differs between sexes, in that females mostly utter contact(-food) calls, whereas males produce a great number of threat calls. Such difference in vocal usage is associated with social roles, with females being involved in more social tasks within the group and males being responsible for territory defense.
Ultimate mechanisms for sexual dimorphism in primates explain the evolutionary history and functional significance of the sexual dimorphism expressed among primates.
In primates, sexual dimorphism including body size, canine tooth size, and morphological characteristics is often attributed to sexual selection, which is regarded to act through two mechanisms: intrasexual competition and female mate choice.
Most male anthropoid primates increase their potential reproductive output by directly engaging in agonistic (contest) competition for gaining access to females. Any weaponry or other physical characteristics that allow males to win intrasexual combat are therefore strongly favored for the selection. Larger body size has been thought to confer advantages to males in competition for access to females, which is consistent with sexual selection hypothesis. Males with a larger canine tooth also tend to be competitively superior to males with a smaller canine, which explain a dimorphism in canine size between the sexes. For example, baboons are highly dimorphic in both body mass and canine size, where males are actively engaged in fights for increasing their mating success and defending females against other males.
Differential parental investment between the sexes accounts for female mate choice. The number of offspring produced by female primates is often limited due to the small litter size, long intervals between births, relatively slow-growing offspring, and energetically expensive costs of pregnancy, lactation, and child care. Females thus choose their mates possessing certain preferable traits, which could possibly provide genetic or direct phenotypic benefits. For example, the large mane found in male gelada (Theropithecus) is assumed to be a preferable pelage condition favored by females, who primarily control and select their mates. Such preference leads the increase in size dimorphism across primate species, which may be favorable in an environment where resources are limited.
A strong association between polygynous mating system and dimorphism in primates has been observed. Monogamous species tend to show lower degree of sexual dimorphism than polygynous species, since monogamous males have a lower differential reproductive success. Monogamous mating system seems to account for minimal dimorphism in hylobatids, in which females are codominant with males. As an exception, among polygynous primates, colobines as a group consistently exhibit a low level of sexual size dimorphism for unclear reasons. In terms of canine dimorphism, males in polygynous species tend to have larger and relatively stronger canines than males in monogamous and polyandrous species.
Similar magnitudes of body weight dimorphism have been observed in all species within several taxonomic groups such as callitrichids, hylobatids, Cercopithecus, and Macaca.  Such correlation between phylogenetic relatedness and sexual dimorphism across different groups reflects similarities in their behaviors and ecological conditions, but not in independent adaptations. This idea is referred to as “phylogenetic niche conservatism."
Terrestrial primates tend to show a greater degree of dimorphism than arboreal primates. It has been hypothesized that larger sizes of body mass and canine tooth are favored among males of terrestrial primates due to the likelihood of higher vulnerability to predators. Another hypothesis suggests that arboreal primates have limitations on their upper body size, given that larger body size could disrupt their usage of terminal branches for locomotion. However, among some species of guenons (Cercopithecus), arboreal blue monkeys (C. mitis) appear to be more sexually dimorphic than terrestrial vervet monkeys (C. aethiops).
It has been hypothesized that niche divergence between the sexes attributes to the evolution of size dimorphism in primates. Males and females are known to have different preferences for ecological habitat due to different reproductive activities, which could possibly lead to dietary differences, followed by dimorphic morphological traits. This niche divergence hypothesis, however, has never been strongly supported due to the lack of compelling data.
- Flores D, Casinos A. 2011. Cranial ontogeny and sexual dimorphism in two New World monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae). Journal of Morphology 272: 744-757.
- Plavcan JM. 2001. Sexual dimorphism in primate evolution. American Journal of Physical Anthropology 33:25-53.
- Dunham AE, Maitner BS, Razafindratsima OH, Simmons MC, Roy CL. 2013. Body size and sexual size dimorphism in primates: influence of climate and net primary productivity. Journal of Evolutionary Biology 26: 2312-2320.
- Dixson A, Dixson B, Anderson M. 2005. Sexual selection and the evolution of visually conspicuous sexually dimorphic traits in male monkeys, apes, and human beings. Annual Review of Sex Research 16:1-19.
- Gordon AD. 2006. Scaling of size and dimorphism in Primates II: Macroevolution. International Journal of Primatology 27(1):63-105.
- Lindenfors P, Tullberg BS. 1998. Phylogenetic analyses of primate size evolution: the consequences of sexual selection. Biological Journal of the Linnean Society 64:413-447.
- Thoren S, Lindenfors P, Kappeler PM. 2006. Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size. American Journal of Physical Anthropology 130:50-59.
- Kinzey WG. 1972. Canine teeth of the monkey, Callicebus moloch: lack of sexual dimorphism. Primates 13(4):365-369.
- Gingerich PD, Schoeninger MJ. 1979. Patterns of tooth size variability in the dentition of primates. American Journal of Physical Anthropology 51(3):457-465.
- Hens SM. 2005. Ontogeny of craniofacial sexual dimorphism in the orangutan (Pongo pygmaeus). I: Face and palate. American Journal of Primatology 65:149-166.
- Berge C, Penin X.2004. Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional procrustes analysis. American Journal of Physical Anthropology 124:124-138.
- Schultz AH. 1962. Metric age changes and sex differences in primate skull. Zeitschrift fur Morphologie und Anthropologie 52(3):239-255.
- Wood BA. 1976. The nature and basis of sexual dimorphism in the primate skeleton. Journal of Zoology 180(1):15-34.
- Setchell JM, Wickings EJ. 2005. Dominance, status signals, and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25-50.
- Plavcan JM. 2012. Sexual size dimorphism, canine dimorphism, and male-male competition in primates: where do humans fit in? Human Nature 23:45-67.
- Stone AI. 2014. Is fatter sexier? Reproductive strategies of male squirrel monkeys (Saimiri sciureus). International Journal of Primatology 35:628-642.
- Bouchet H, Blois-Heulin C, Lemasson A. 2012. Age- and sex-specific patterns of vocal behavior in De Brazza’s monkeys (Cercopithecus neglectus). American Journal of Primatology 74:12-28.
- Bouchet H, Pellier A, Blois-Heulin C, Lemasson A. 2010. Sex differences in the vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus): A multi-level acoustic analysis. American Journal of Primatology 72:360-375.
- Watkins GG. 1996. Proximate causes of sexual size dimorphism in the Iguanian lizard Microlophus occipitalis. Ecology 77(5):1473-1482.
- Plavcan JM, Van Schaik CP. 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology 103:37-68.
- Mitani JC, Gros-Louis J, Richards AF. 1996. Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. The American Naturalist 147(6):966-980.
- Craul M, Zimmermann E, Radespiel U. 2004. First experimental evidence for female mate choice in a nocturnal primate. Primate 45:271-274.
- Muller MN, Thompson ME, Kahlenberg SM, Wrangham RW. 2011. Sexual coercion by male chimpanzees show that female choice may be more apparent than real. Behavioral Ecology and Sociobiology 65:921-933.
- Leigh SR, Shea BT. 1995. Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology 36:37-60.
- Plavcan JM, Ruff CB. 2008. Canine size, shape, and bending strength in primates and carnivores. American Journal of Physical Anthropology 136:65-84.
- Cardini A, Elton S. 2008. Variation in guenon skulls (II): sexual dimorphism. Journal of Human Evolution 54:638-647.
- Shine R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. The Quarterly Review of Biology 64(4):419-461.