Sexual dimorphism in non-human primates

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Hamadryas baboon female (left) and male (right)
Black howler monkey
female (left) and male (right)

tarsiers are monomorphic.[2]

Sexual dimorphism can manifest itself in many different forms. In male and female primates there are obvious physical difference such as body size or canine size. Dimorphism can also be seen in skeletal features such as the shape of the pelvis or the robustness of the skeleton.[3] There are two mating systems in the sexual selection of primates.

Types

Body size

Extant primates exhibit a broad range of variation in sexual size dimorphism (SSD), or sexual divergence in body size.

proboscis monkeys.[2][5]
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,
callitrichine and strepsirrhine primates are, however, characterized by the reverse dimorphism, a phenomenon in which females are larger than males.[2]

Tooth size

Canine sexual dimorphism is one particular type of sexual dimorphism, in which males of a species have larger

Callicebus moloch), for instance, do not exhibit any differences in the size of canine teeth between the sexes.[7]

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.[8] A canine dimorphism is also more widely seen in maxillary canines than in mandibular canines.[2]

Craniofacial structure

Craniofacial sex differentiation among anthropoid primates varies in a wide range and is known to arise primarily through

spider monkeys and gibbons the sex differences is on a general average about 4 to 5 percent.[11] 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).[9]

Skeletal structure

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.

howler monkeys, which contribute to the resonation of their voices.[2]

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.[2] 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.[5] Studies have shown that male color in mandrills serves as a badge of social status in the species.[13]

Temporary sexual dimorphism

Some sexual dimorphic traits in primates are known to appear on a temporary basis. In

female choice for larger males.[14][15]
Orangutan males tend to gain weight and develop large cheek flanges, when they achieve dominance over other group members.[14]

Vocalization

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.

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.[16]

Ultimate mechanisms

Ultimate mechanisms explain the evolutionary history and functional significance of the sexual dimorphism expressed among primates.[18]

Intrasexual selection

Intrasexual selection is one of two components that make up sexual selection as defined by Darwin and refers to competition within a sex for access to mates.[2] For species where such competition determines their reproductive success, selection pressures for increased strength/size and weaponry/canines are heightened, resulting in the evolution of sexual dimorphism.[2] The most common illustration of intrasexual selection is male–male competition, in which males of a species fight or threaten each other for preferential access to females.[2]

A prime example of intrasexual selection can be found in baboons. Male baboons are known to violently fight and threaten each other over females and show high levels of sexual dimorphism in body and canine size, both of which are assumed to aid in combat.[2] The “winners” of such interactions mate with the desired female and produce offspring, passing their traits to the next generation, while unsuccessful males are excluded from mating.[2] As a result, traits beneficial to fighting are selected for in the population over time.[2]

Intrasexual selection also operates through female–female competition.[2] Female howler monkeys, for example, experience frequent agonistic encounters both within and between coalitions.[2] One possible evolutionary explanation for female–female competition in red howler monkeys is its role as a counter-strategy to infanticide through group size regulation (by evicting other females).[2][19] Instances of female–female competition such as this could potentially select for greater body and/or canine size in females, as well as reduce the pressure for those same traits in males by limiting the occurrence of male–male competition (as group size regulation reduces the likelihood of threats/takeovers by immigrant males), overall reducing dimorphism.[2]

Intersexual selection

Intersexual selection is often represented by female choice, but more generally refers to differential preferences one sex has for individuals of the opposite sex, including sexual coercion of females by males. Sexual dimorphism arises via intersexual selection most often through female preference for certain male secondary sexual characteristics, but can also arise as a result of males' selective pressure to physically overpower females he wishes to mate with.[2] Gamete production, gestation, lactation, and infant care are all highly energetically costly processes for females, so these energy and time constraints would lead them to choose—when possible—mates with higher quality genes leading to higher quality offspring with a better chance of survival and reproductive success.[2] Importantly, what is deemed “high quality” by the female in this instance need not confer a survival advantage to the male, but must be perceived by females as a sign of attractiveness if not health.[2] A common example of this is sexually dimorphic coloration.[2]

In rhesus macaques, red facial coloration is attractive to females to the point of influencing the reproductive success of high-ranking males.[20] To be deemed a sexually selected trait said trait must be heritable and confer a reproductive advantage.[20] In this example, facial redness is heritable, but only increases a male's reproductive success if he is also high-ranking, and rank is not determined by facial redness (dominance in rhesus macaques is not competition-based but rather queue-based).[20][21] While this trait is believed to be the result of intersexual selection, such examples demonstrate the complex nature of determining evolutionary explanations for sexually dimorphic characteristics.

Paternity confusion is another component of female choice. By actively seeking out matings with newly immigrated males, females produce offspring whose fathers are unknown. This is beneficial to females because it allows them to sire offspring without the risk of infanticide.[2] These “sneaky matings” mean that even if a male “wins” the opportunity to mate with a female, the father of her infant is not necessarily determined by the outcome of male–male competition, thus limiting the reproductive benefits associated with such competition and dampening the pressure for sexually selected dimorphic traits.[2]

Mating systems

In

colobines as a group consistently exhibit a low level of sexual size dimorphism for unclear reasons.[22] Gibbons, on the other hand, are an example of monogamous primates that can be described as “monomorphic,” meaning males and females appear the same with little to no sexual dimorphism.[2] The correlation between mating system and dimorphism in haplorhines likely indicates sexual selection is the driving force behind dimorphism in species of this suborder. Another more general trend observed in haplorhines is a correlation between body mass dimorphism with overall body size.[2]

The lack of a clear relationship between mating system and intensity of sexual dimorphism in strepsirrhines remains a mystery, with some explanations ranging from ecological constraints to selection for speed and agility to unique instances of female social dominance (such as in lemurs) reducing dimorphism.[2] One study offers a challenge to the argument that environmental constraints are the main factor driving monomorphism on Madagascar but fails to isolate specific factors to substitute this theory; simply put, there is no consensus on why strepsirrhines do not follow similar patterns to haplorhines.[4]

Phylogeny

Similar magnitudes of body weight dimorphism have been observed in all species within several taxonomic groups such as callitrichids, hylobatids, Cercopithecus, and Macaca.[22] 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."[22]

Terrestriality

vervet monkeys (C. aethiops).[23]

Niche divergence

It has been hypothesized that niche divergence between the sexes attributes to the evolution of size dimorphism in primates.[2] 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.[24] This niche divergence hypothesis, however, has never been strongly supported due to the lack of compelling data.[2]

See also

References

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  6. ^ Gordon, A. D. (2006). "Scaling of size and dimorphism in Primates II: Macroevolution". International Journal of Primatology. 27 (1): 63–105.
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  16. ^ a b 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.
  17. ^ 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.
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  24. ^ 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.

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