Sexual dimorphism in non-human primates

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Hamadryas baboon female (left) and male (right) Papio hamadryas pair.jpg
Hamadryas baboon female (left) and male (right)
Black howler monkey female (left) and male (right) Howler monkey.jpg
Black howler monkey female (left) and male (right)

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. [1] However, such sex differences are primarily limited to the anthropoid primates; most of the strepsirrhine primates (lemurs and lorises) and tarsiers are monomorphic. [2]

Contents

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. [4] 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. [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, [6] counteracted by fecundity selection on the other sex. Some 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 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. [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 ontogenetic processes. [9] 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. [10] 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. [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. [2] [12] 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. [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 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. [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. [16] 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. [17] 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. [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 haplorhines, the degree to which intrasexual and intersexual selection drive sexual dimorphism is dependent on the social organization and mating system of a particular species. Phylogenetic studies reveal polygynous systems among haplorhines show elevated levels of dimorphism. This is expected because polygynous groups, i.e. single-male multi-female, imply males can monopolize females, suggesting male–male competition plays an important role in ensuring any opportunity to reproduce. Without somewhat guaranteed access to females—as is the case in monogamous primates—a male's lifetime reproductive output is dependent on his ability to outcompete other males and lead a group of females. As an exception, among polygynous primates, 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

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. [2] However, among some species of guenons (Cercopithecus), arboreal blue monkeys (C. mitis) appear to be more sexually dimorphic than terrestrial 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

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

Sexual selection is a mode of natural selection in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.

<span class="mw-page-title-main">Sex</span> Trait that determines an organisms sexually reproductive function

Sex is the trait that determines whether a sexually reproducing organism produces male or female gametes. During sexual reproduction, a male and a female gamete fuse to form a zygote, which develops into an offspring that inherits traits from each parent. By convention, organisms that produce smaller, more mobile gametes are called male, while organisms that produce produce larger, non-mobile gametes are called female. An organism that produces both types of gamete is hermaphrodite.

<span class="mw-page-title-main">Sexual dimorphism</span> Condition where males and females exhibit different characteristics

Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, particularly characteristics not directly involved in reproduction. The condition occurs in most dioecious species, which consist of most animals and some plants. Differences may include secondary sex characteristics, size, weight, color, markings, or behavioral or cognitive traits. Male-male reproductive competition has evolved a diverse array of sexually dimorphic traits. Aggressive utility traits such as "battle" teeth and blunt heads reinforced as battering rams are used as weapons in aggressive interactions between rivals. Passive displays such as ornamental feathering or song-calling have also evolved mainly through sexual selection. These differences may be subtle or exaggerated and may be subjected to sexual selection and natural selection. The opposite of dimorphism is monomorphism, when both biological sexes are phenotypically indistinguishable from each other.

<span class="mw-page-title-main">Strepsirrhini</span> Suborder of primates

Strepsirrhini or Strepsirhini is a suborder of primates that includes the lemuriform primates, which consist of the lemurs of Madagascar, galagos ("bushbabies") and pottos from Africa, and the lorises from India and southeast Asia. Collectively they are referred to as strepsirrhines. Also belonging to the suborder are the extinct adapiform primates which thrived during the Eocene in Europe, North America, and Asia, but disappeared from most of the Northern Hemisphere as the climate cooled. Adapiforms are sometimes referred to as being "lemur-like", although the diversity of both lemurs and adapiforms does not support this comparison.

<span class="mw-page-title-main">Mandrill</span> Species of Old World monkey from Africa

The mandrill is a large Old World monkey native to west central Africa. It is one of the most colorful mammals in the world, with red and blue skin on its face and posterior. The species is sexually dimorphic, as males have a larger body, longer canine teeth and brighter coloring. It is the largest monkey in the world. Its closest living relative is the drill, with which it shares the genus Mandrillus. Both species were traditionally thought to be baboons, but further evidence has shown that they are more closely related to white-eyelid mangabeys.

<i>Mandrillus</i> Genus of Old World monkeys

Mandrillus is a genus of large Old World monkeys distributed throughout central and southern Africa, consisting of two species: M. sphinx and M. leucophaeus, the mandrill and drill, respectively. Mandrillus, originally placed under the genus Papio as a type of baboon, is closely related to the genus Cercocebus. They are characterised by their large builds, elongated snouts with furrows on each side, and stub tails. Both species occupy the west central region of Africa and live primarily on the ground. They are frugivores, consuming both meat and plants, with a preference for plants. M. sphinx is classified as vulnerable and M. leucophaeus as endangered on the IUCN Red List of Threatened Species.

<span class="mw-page-title-main">Anisogamy</span> Sexual reproduction involving a large, female gamete and a small, male gamete

Anisogamy is a form of sexual reproduction that involves the union or fusion of two gametes that differ in size and/or form. The smaller gamete is male, a sperm cell, whereas the larger gamete is female, typically an egg cell. Anisogamy is predominant among multicellular organisms. In both plants and animals gamete size difference is the fundamental difference between females and males.

<span class="mw-page-title-main">Parental investment</span> Parental expenditure (e.g. time, energy, resources) that benefits offspring

Parental investment, in evolutionary biology and evolutionary psychology, is any parental expenditure that benefits offspring. Parental investment may be performed by both males and females, females alone or males alone. Care can be provided at any stage of the offspring's life, from pre-natal to post-natal.

Monogamous pairing in animals refers to the natural history of mating systems in which species pair bond to raise offspring. This is associated, usually implicitly, with sexual monogamy.

Rensch's rule is a biological rule on allometrics, concerning the relationship between the extent of sexual size dimorphism and which sex is larger. Across species within a lineage, size dimorphism increases with increasing body size when the male is the larger sex, and decreases with increasing average body size when the female is the larger sex. The rule was proposed by the evolutionary biologist Bernhard Rensch in 1950.

<i>Hetaerina</i> Genus of damselflies

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<span class="mw-page-title-main">Sexual selection in humans</span> Evolutionary effects of sexual selection on humans

Sexual selection in humans concerns the concept of sexual selection, introduced by Charles Darwin as an element of his theory of natural selection, as it affects humans. Sexual selection is a biological way one sex chooses a mate for the best reproductive success. Most compete with others of the same sex for the best mate to contribute their genome for future generations. This has shaped human evolution for many years, but reasons why humans choose their mates are not fully understood. Sexual selection is quite different in non-human animals than humans as they feel more of the evolutionary pressures to reproduce and can easily reject a mate. The role of sexual selection in human evolution has not been firmly established although neoteny has been cited as being caused by human sexual selection. It has been suggested that sexual selection played a part in the evolution of the anatomically modern human brain, i.e. the structures responsible for social intelligence underwent positive selection as a sexual ornamentation to be used in courtship rather than for survival itself, and that it has developed in ways outlined by Ronald Fisher in the Fisherian runaway model. Fisher also stated that the development of sexual selection was "more favourable" in humans.

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<span class="mw-page-title-main">Gracile capuchin monkey</span> Genus of mammals belonging to the capuchin and squirrel monkey family of primates

Gracile capuchin monkeys are capuchin monkeys in the genus Cebus. At one time all capuchin monkeys were included within the genus Cebus. In 2011, Jessica Lynch Alfaro et al. proposed splitting the genus between the robust capuchin monkeys, such as the tufted capuchin, and the gracile capuchins. The gracile capuchins retain the genus name Cebus, while the robust species have been transferred to Sapajus.

<span class="mw-page-title-main">Sexual selection in birds</span>

Sexual selection in birds concerns how birds have evolved a variety of mating behaviors, with the peacock tail being perhaps the most famous example of sexual selection and the Fisherian runaway. Commonly occurring sexual dimorphisms such as size and color differences are energetically costly attributes that signal competitive breeding situations. Many types of avian sexual selection have been identified; intersexual selection, also known as female choice; and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Sexually selected traits often evolve to become more pronounced in competitive breeding situations until the trait begins to limit the individual's fitness. Conflicts between an individual fitness and signaling adaptations ensure that sexually selected ornaments such as plumage coloration and courtship behavior are "honest" traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviors.

<span class="mw-page-title-main">Sexual selection in mammals</span> Mode of natural selection

Sexual selection in mammals is a process the study of which started with Charles Darwin's observations concerning sexual selection, including sexual selection in humans, and in other mammals, consisting of male–male competition and mate choice that mold the development of future phenotypes in a population for a given species.

<span class="mw-page-title-main">Sexual selection in amphibians</span> Choice of and competition for mates

Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.

Sexual selection is described as natural selection arising through preference by one sex for certain characteristics in individuals of the other sex. Sexual selection is a common concept in animal evolution but, with plants, it is oftentimes overlooked because many plants are hermaphrodites. Flowering plants show many characteristics that are often sexually selected for. For example, flower symmetry, nectar production, floral structure, and inflorescences are just a few of the many secondary sex characteristics acted upon by sexual selection. Sexual dimorphisms and reproductive organs can also be affected by sexual selection in flowering plants.

<span class="mw-page-title-main">Sexual dimorphism in Carnivorans</span> The sexual dimorphism seen in Carnivorans

Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, particularly characteristics not directly involved in reproduction. Sexual dimorphism in carnivorans, in which males are larger than females, is common among carnivorans. Sexual selection is frequently cited as the cause of the intraspecific divergence in body proportions and craniomandibular morphology between the sexes within the Carnivora order. It is anticipated that animals with polygynous mating systems and high levels of territoriality and solitary behavior will exhibit the highest levels of sexual size dimorphism. Pinnipeds offer an illustration for this.

References

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