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Mating Systems MEGAN PETERSDORF and JAMES P. HIGHAM New York University, United States
Primates are an extraordinary group of mammals. While many mammalian orders exhibit relatively little intra-order variation in social and mating systems, primates are renowned for the diversity of their social and reproductive organization and patterns. This entry describes and discusses the variation in primate mating systems, with an emphasis on observed diversity, and the factors that may explain it.
What Constitutes a Mating System? A mating system reflects the distribution of reproduction across sexually active adult members of a social unit, whereas a social system is defined by the composition and grouping patterns of individuals. It is important to distinguish between these two different systems, as although they may map onto each other, they are not necessarily congruent, and different selection pressures have shaped the evolution of the two system types (Kappeler and van Schaik 2002). Mating systems describe the number of mates acquired, how they are acquired, and the associated patterns of parental care. The defining feature of a mating system is how the distribution of mating within a social unit leads to variance in reproductive success between and among males and females. As mating systems evolve as a result of the outcome of competition between individuals to maximize their reproductive success, they are inevitably linked to individual reproductive strategies shaped by sexual selection. Thus an understanding of variation in reproductive strategies and success between sexes and among individuals of the same sex is a critical part of understanding variation in mating systems.
Although the majority of mammalian orders tend to exhibit one or a few main mating systems, the Primates are noted for their remarkable diversity of mating systems, namely monogamy, polyandry, polygyny, and polygynandry. Differences in mating systems are created by variation in the potential of males to monopolize access to females, and can be understood by considering the vast differences in reproductive potential between male and female mammals (Clutton-Brock 1989). These differences are also at the heart of attempts to explain primate social systems and styles (see entry “Socioecological Model”). In these models, predation risk and food availability influence female distributions, with male distributions then following suit according to males’ best strategies for maximizing reproductive success. This is based on Bateman’s principle (Bateman 1948) that female reproduction is limited by access to the physical resources they need to reproduce (i.e., food), while male reproductive success is limited by access to fertile females. The operational sex ratio (the ratio of fertile females to sexually active males) that emerges is a measure of the degree to which males can monopolize reproduction with females. The degree to which any one male can successfully defend exclusive mating access with females results in variation in the intensity of sexual selection mechanisms (intrasexual competition, mate choice, sexual conflict), which ultimately explains the variation we see among and within different mating systems.
Monogamy Monogamy is characterized by one female mating with one male. The potential for males to monopolize multiple females is typically low due to widespread female spatial distribution and/or paternal care that is obligatory to offspring survival, creating a situation where the two sexes generally have equal variance in reproductive success. In monogamous mating systems, males forego higher reproductive potential to ensure the
The International Encyclopedia of Primatology. Edited by Agustín Fuentes. © 2017 John Wiley & Sons, Inc. Published 2017 by John Wiley & Sons, Inc. DOI: 10.1002/9781119179313.wbprim0212
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paternity and survival of their offspring. There is often parental investment by both sexes, either directly (e.g., infant carrying in callitrichids) or indirectly (e.g., territorial defense in hylobatids). Males and females are typically sexually monomorphic in size, as a result of less intense male–male competition over females. It is difficult to disentangle whether social and sexual monogamy is congruent in many species, due to a lack of genetic data from wild populations. It is likely that most species are socially but not completely sexually monogamous, as extrapair copulations and polyandry are found in many species. Primates with primarily monogamous mating systems include indri (Indri), owl monkeys (Aotus), titi monkeys (Callicebus), some marmosets and tamarins (family Callitrichidae), and siamangs and gibbons (family Hylobatidae). Monogamy is not yet known from Old World monkeys.
systems, intrasexual competition is usually more intense between the breeding female and other group females, as evidenced by reproductive suppression of subordinate females by the alpha female in callitrichids (see entry “Reproductive Suppression”). Genetic data are not yet available for many species that exhibit polyandry, so it is often unknown how paternity is allocated across different males. Postcopulatory mechanisms of sexual selection, such as sperm competition and/or cryptic female choice, seem likely to occur, making observations of matings potentially poor indicators of reproductive success. Facultative polyandry is only found in some species (and for some species only in certain populations) of callitrichids, some lemur species (e.g. cheirogaleids), as well as in some populations of the Sumatran siamang (Symphalangus syndactylus).
Polygyny Polyandry Polyandry occurs when one female mates with multiple males, but where each male only mates with that one female. Females have higher variance in reproductive success than males, since reproduction is skewed towards a single breeding female, but is spread more evenly among males. As in other orders of mammals, this mating system is rare in primates, and only occurs as a secondary mating system (with monogamy as primary, see above). This “facultative polyandry” results in two or more males copulating with a female and cooperating to help rear her offspring. As in monogamy, male monopolization potential of multiple females is low due to the constraint of obligatory paternal care. In some callitrichids, polyandry may be adaptive due to rapid reproductive rates and the evolution of twin births. As females need help to carry and care for twins, they need help from mating partners (though help may also come from female relatives; see entry “Cooperative Breeding”). Cooperative polyandry can also result if the female needs a larger territory for successful reproduction than a single male can defend, in which case a second male will be tolerated by the first, in order to assist with resource defense. In such
Polygynous mating systems are characterized by a single male that mates with multiple females, with those females primarily mating only with him. Due to the physiological constraints of gestation and lactation, primates (like most mammals) require high levels of maternal care, often without the need for paternal care, to ensure offspring survival. In combination with a spatiotemporal distribution of females that allows one male to monopolize multiple females, this allows males to capitalize on the potential for polygyny, in which variance in male reproductive success is greater than variance in female reproductive success. Male–male competition over the position of breeding male is intense in polygynous mating systems, resulting in extreme sexual dimorphism in body and canine size, and conspicuous sexually selected traits that may signal competitive ability to other males and/or directly assist in competition with males or in the coercion of females. Due to a lack of mating by other males, sperm competition is expected to be low, and, consistent with this, males living in polygynous mating systems tend to have small testes relative to body size. For females, polygyny can be beneficial, as they may gain indirect (e.g., genetic) or direct (e.g., protection, access to food resources) benefits for themselves and their offspring from
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mating with a single male. Since a single male is able to monopolize reproduction with multiple females, this can create extreme variance in reproductive skew among males of a population. Depending on whether females are group living or solitary, male monopolization of reproduction is accomplished through different mechanisms. Solitary species exhibit spatial polygyny, in which a male’s territory overlaps with multiple solitary females’ home ranges, which he can patrol and defend. This system is found mostly in nocturnal solitary strepsirhines (e.g., white-footed sportive lemur: Lepilemur leucopus). Depending on the distribution and size of female territories, there may also be intraspecific variation that results in either spatial polygyny or monogamous mating systems (e.g., Demidoff ’s galago: Galago demidoff). More common in diurnal group-living primates is female-defense (or harem) polygyny. This can also take slightly different forms, depending on the population’s social organization. One-male groups can occur as units with spatially separate home ranges (e.g., black-andwhite colobus: Colobus guereza; gorillas: Gorilla spp.; most leaf monkeys: Trachypithecus spp.) or within a multilevel society (e.g., hamadryas baboons: Papio hamadryas; geladas: Theropithecus gelada). Though both species exhibit similar multilevel societies with polygynous groups as their base unit, the males of hamadryas baboons and gelada obtain their females in different ways. Hamadryas form one-male units for themselves by collecting and defending unrelated females one by one, whereas gelada males overtake established female-bonded groups. Absolute polygyny with no extragroup copulations or paternities is rare, as populations are often not impermeable to female matings with external males. Other males may, however, achieve reproductive success through alternative strategies. For example, hamadryas and gelada units often include a follower male that may obtain sneak matings and possibly later take over the group. Additionally, there may be seasonal multi-male influxes into one-male units during the breeding season, as seen in many species of guenons (Cercopithecus spp.) and patas monkeys (Erythrocebus patas), resulting in functional polygynandry (see below).
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Polygynous mating systems can be excellent examples of how mating systems do not always match social organizations. Red howler monkeys (Alouatta seniculus) live in multi-male groups, but a single male sires all offspring. Hanuman langurs (Semnopithecus entellus) occur in multi-male and one-male groups in different geographic locations, such that one species with the same social organization may not always be characterized by a single mating system. Even within groups of gorillas, considered a classical polygynous species, there may be multiple males that sire offspring. Often, but not always, these other-male copulations and paternities can be attributed to the fact that males may form kin-based groups, such that extramale reproduction still increases the primary male’s inclusive fitness. Without genetic information on kinship and paternity, it is difficult to distinguish kin-based groups from unrelated multi-male groups, how paternity is ultimately allocated among them, and what the fitness consequences are for the primary male.
Polygynandry When a single male cannot defend exclusive access to females due to the presence of a large number of females (because females are spatially dispersed and/or because of high levels of reproductive synchrony), multiple males mate with group females, resulting in polygynandry. In a polygynandrous mating system, males and females both mate with multiple partners. However, within this system there is a great amount of intra- and interspecific variation in intrasexual reproductive success. While this system has often been called “promiscuous,” mating is far from indiscriminate, as both male and female reproductive strategies play a role in determining mating partners. The number of males in a group is generally correlated with the number of females. As group size increases, males will share mating with other males, either due to their inability to exclude unrelated males from mating with females, or because they form cooperative alliances with related males to defend a territory that includes females. The former is the more common form of polygynandry (e.g., Macaca spp.), while the latter
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is characteristic of chimpanzees (Pan troglodytes). Similar to polygyny, in polygynandry the variance in male reproductive success is greater than the variance in female reproductive success. There is, however, a range of variation in the monopolization potential among males of different species and populations. Whereas in other systems, understanding the monopolization potential is often enough to define the reproductive outcomes for the mating system, within polygynandry, understanding the variation in this potential and its interaction with sexual selection mechanisms is the only way to understand intrasexual variation in reproductive skew. Within many group-living polygynandrous systems (e.g., papionins), monopolization potential is strongly influenced by dominance rank, but in varying degrees, depending on the taxa. Often, there can be high skew in male mating success as a function of dominance rank, according to the Priority-of-Access model (Altmann 1962). Reproductive success may or may not follow a similar pattern, depending on the importance of sneak copulations and postcopulatory mechanisms of reproductive competition, such as sperm competition. Related to this may be the species’ mode of dominance acquisition (top- versus bottomentry; van Noordwijk and van Schaik 2004). The variation in monopolization potential affects the type and intensity of sexual selection that acts on individuals in a population, which acts as a feedback loop on monopolization potential. If the potential for a male to monopolize reproduction is high, males will fight over access to females directly through contest competition, and females will choose mates of high dominance rank, reinforcing the high reproductive skew (similar to polygyny). If the monopolization potential is low, males may compete over females indirectly via sperm competition, and females may compete with each other over males and will choose mates based on male quality (as signaled through sexually selected traits). Differences in these processes result in great variation in the degree of sexual dimorphism in body and canine size, as well as in relative testes size, within polygynandrous species. On average, however, polygynandrous species are more sexually dimorphic in body and canine size than monogamous
species, and have larger relative testes size than monogamous and polygynous species. Polygynandry also occurs in dispersed nongregarious species, such as orangutans (Pongo spp.), and may also occur in many nocturnal strepsirhines (e.g., mouse lemurs: Microcebus spp.; aye-ayes: Daubentonia; galagos: Galago spp.). While it is difficult to observe matings—and hence to confirm polygynandry—in these nocturnal strepsirhines, it seems unlikely that they are polygynous, due to the difficulty males have in monopolizing females in such a dispersed system. Owing to their unique feeding ecology, orangutans are the only diurnal primates with a nongregarious dispersed social organization. While it was long thought that orangutans had a polygynous mating system, with high reproductive skew in favor of flanged males, it is now apparent that females may choose to mate with both morphs, and that flanged and unflanged males may experience similar reproductive success through different routes. Polygynandry is the most common mating system in primates, and is found across the primates in strepsirhines (e.g., ring-tailed lemurs: Lemur catta; nocturnal strepsirhines: see above), New World monkeys (e.g., squirrel monkeys: Saimiri spp.; capuchins: Cebus spp.; spider monkeys: Ateles spp.), Old World monkeys (e.g., baboons: Papio spp.; macaques: Macaca; mandrills: Mandrillus sphinx), and great apes (e.g., chimpanzees and bonobos: Pan spp.).
Conclusions Differential sexual selection pressures not only have led to marked variation among primate mating systems, but also help to explain the remarkable variation in key characteristics within mating systems, such as the degree to which males can monopolize female reproduction within polygynandrous systems (i.e., reproductive skew). In turn, this influences variation in other factors such as the mode of dominance acquisition, the type and intensity of male–male competition (direct vs indirect), the degree and type of both female and male mate choice, levels of sexual dimorphism, and the form and function of sexually selected traits. A holistic understanding
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of the distribution and concomitant variation of all these characteristics requires an understanding of how different sexual selection processes have combined during species evolution.
SEE ALSO: Mating Patterns; Monogamy; Paternal Care; Promiscuous Mating; Reproductive Success; Reproductive Synchrony; Sexual Selection; Socioecological Model; Social System (Social Structure)
REFERENCES Altmann, Stuart A. 1962. “A Field Study of the Sociobiology of Rhesus Monkeys, Macaca mulatta.” Annals of the New York Academy of Sciences, 102: 338–435. DOI:10.1111/j.1749-6632.1962.tb13650.x. Bateman, Angus J. 1948. “Intra-Sexual Selection in Drosophila.” Heredity, 2: 349–368. DOI:10.1038/ hdy.1948.21. Clutton-Brock, Tim H. 1989. “Mammalian Mating Systems.” Proceedings of the Royal Society B: Biological Sciences, 236(1285): 339–372. DOI:10.1098/ rspb.1989.0027. Kappeler, Peter M., and Carel P. van Schaik. 2002. “Evolution of Primate Social Systems.” International Journal of Primatology, 23(4): 707–740. DOI:10.1023/A:1015520830318.
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van Noordwijk, Maria A., and Carel P. van Schaik. 2004. “Sexual Selection and the Careers of Primate Males: Paternity Concentration, Dominance Acquisition Tactics and Transfer Decisions.” In Sexual Selection in Primates: New and Comparative Perspectives, edited by Peter M. Kappeler and Carel P. van Schaik, 208–229. Cambridge: Cambridge University Press.
FURTHER READING Davies, Nicholas B., John R. Krebs, and Stuart A. West. 2012. “Mating Systems.” In An Introduction to Behavioral Ecology, 4th ed., edited by Nicholas B. Davies and John R. Krebs, 254–281. Chichester: WileyBlackwell. Dixson, Alan F. 2012. Primate Sexuality, 2nd ed. Oxford: Oxford University Press. Emlen, Stephen T., and Lewis W. Oring. 1977. “Ecology, Sexual Selection, and the Evolution of Mating Systems.” Science, 197(4300): 215–223. DOI:10.1126/science.327542. Kappeler, Peter M., and Carel P. van Schaik. 2004. Sexual Selection in Primates: New and Comparative Perspectives. Cambridge: Cambridge University Press.
