Sexual dimorphism in non-human primates

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Sexual dimorphism describes the morphological, physiological and behavioral differences between male and females of the same species. Primates, including lemurs, monkeys, and apes, show various degrees of sexual dimorphism.

Types[edit]

Body size[edit]

Male body size is generally larger than females due to differences in weight and muscular development. This is true for most species of primates, but there are exceptions in cases like the gibbon where the male and female body sizes are similar.[1] Larger species like the gorilla tend to be more dimorphic than smaller species like New World monkeys and Old World Colobines.[2]

Tooth size[edit]

The most variation between tooth sizes occurs in the canine region, with incisors being somewhat variable, and the cheek region (premolars and molars) being the least. Anthropoid primate male canines have been measured to be almost four times taller than those in females. In Old World Monkeys, with the exception of the Yellow Baboon, deciduous teeth showed no significant size dimorphism.[3][4]

Cranial structure[edit]

See also: Allometry

Ontogenetic scaling explains the differences in craniofacial (skull) morphology by measuring the changes in the cranium size relative to the body size during development, in both males and females.[5] Results of univariate and multivariate analyses were used to find small differences in the dimensions of the viscerocranium of Liberian chimpanzees.[6] In the common chimpanzee, Pan troglodytes, the male skulls were on average 3.7% larger than those of females.[7] Overall, studies on species like the baboon have shown that females and males share the same growth trajectory, although ending at different points, accounting for differences in facial size.[6][8]

Pelage color and markings[edit]

Main article: Fur

Color and marking differences among males and females often occur on the face.[9] However, they can occur in other areas around the chest and back; for example, in the silverback gorilla, males acquire silver patches across their backs and upper thighs at sexual maturity. In the genus Mandrillus, the males have a red stripe under the lower lip, red on the penis and above the groin, and blue, violet, and pink colors on the rump and genitals. The high coloration in males shows high dominance rank and more reproductive success.[10]

Other anatomical features[edit]

Other anatomical features show sexual dimorphism in different primate species, such as the bulbous nose in Nasalis larvatus, and the gular pouch in the Orangutans (Pongo sp). Males may also have permanent skin ridges, baldness, and nuchal or sagittal crests (i.e. silver back gorillas).[9] Some other ornaments include shoulder capes in the hamadryas baboons and cheek flanges in male orangutans.[10]

Temporary sexual dimorphism[edit]

Temporary changes are associated with sexual reproduction. Males experience a skin color change on the scrotum, while females experience sexual swellings in the ischial region due to the ovulation phase of the estrous cycle.[9]

Behavior[edit]

In the cotton-top tamarin (Saguinus oedipus), males react to intruders by using physical aggression, vocalization, and piloerection, while females use scent-marking tactics.[11] In the vervet monkey, males move to other groups when they reach sexual maturity while females remain within the group for their entire life.[12]

Proximate causes[edit]

Proximate causation is how sexual dimorphism is expressed during development[clarification needed].

Diet[edit]

Smaller primates lack the morphological and masticatory traits that allow them to process and digest leaves efficiently. Large species like the colobine monkeys are more folivorus, they do not gain enough nutrients from just being carnivores so they eat leaves for extra protein.[13] Small species require a high quality diet while large ones eat large amounts of low quality food. Since large species are more sexually dimorphic, folivores are more dimorphic than frugivores.[14]

Ultimate causes[edit]

Ultimate causes explain why dimorphism has evolved. These include natural and sexual selection.

Gender roles[edit]

Sexual selection may act on male performance capacity in male-male competition and territorial behaviors. Sexual selection and fecundity also contributes to the differences between size and shape between the sexes.[15] While male features relate more to their competition and finding mates, female features gear towards investment in offspring, timing of mating, and advertisement of sexual readiness at the height of estrus.[9]

Male aggression, chasing and mate guarding have costly effects on feeding efficiency and sleep in species like the golden lion tamarins and wedge-capped capuchins. Since male-male competition has an effect on body maintenance due to high energy costs, a larger body size will be beneficial.[1] Aggression usually occurs in males more than females because of the different rates of reproduction.[16] While trying to dominate other males it will help to have features such as a larger head, more muscle mass and bigger canines. High aggression species have a higher degree of weight dimorphism than low aggression species also showing that body size is favored in competitive environments.[17]

Females use tactics like copulatory calls in mate attraction, mate choice, and during the pressures of sexual selection.[18] They have swelling of the isichial area in order to show their fertility and attractiveness to present males.[19] After mating, females have the most investment in their offspring. This is true in more than 300 non-human primate species with the exception of some monogamous species where the father cares for the offspring.[20] Since this is the case they have less time for competition and therefore a decreased need for features that may be associated with it. Instead females bodies require more energy investment for metabolic processes associated with reproduction, such as lactation and pregnancy, which account for their depressed body size.[21]

Phylogeny[edit]

The degree of sexual dimorphism varies throughout different families and subfamilies of the primate species such Asaotines, Colobines, Atelines, Great apes, and Cercopithecines. Callitrichines, Pithecines, and Hylobatids however, consistently show low levels of sex differences while the cercopithecines show the greatest degree. This is due to factors including their ancestry and environments.[17]

Copulatory plugs[edit]

Copulatory plugs are a passive form of mate guarding, which reduces selection pressure for a larger male size. It is an interference-type sperm competition, meaning it inhibits successful inseminations by other males. This is used in cases where females are very spatially dispersed and have synchronized estrous cycles making it difficult for large males to monopolize and mate with multiple females. In species where copulatory plugs are present there is a smaller degree of sexual dimorphism. This occurs in about 62 primate species including the Haplorrhines.[22]

Mating system[edit]

Polygynous species are more sexually dimorphic than species whose individuals only have one mate.[2] Examples of this are present in the case of New World monkeys like the marmosets. This may be due to a lower amount of sexual selection in monogamous species or because of the differences in escaping predation in both mating systems.[23] An exception to this is in the Colobine species where sexual dimorphism is low, not due to a lack of competition amongst males, but probably because of greater pressure for a larger female body size. It can also be due to factors which limit overall male growth.[17]

Habitat[edit]

Arboreal species tend to be less dimorphic than terrestrial species. A large body size does not guarantee success in male-male competition within arboreal environments.[9] Large body sizes can also have functional disadvantages such as hindered movement, which can be detrimental to the species. In the terrestrial environments on the other hand, being a larger size would be favored because of threats like large bodied predators and increased male-male competition.[17][24] In such species, the task of defending the troop against predators falls exclusively on the males, who have long canines while the females do not. The male orangutan, however, is much larger than the female, for reasons unknown.

See also[edit]

References[edit]

  1. ^ a b Key, Catherine; Ross, Caroline (1999). "Sex differences in energy expenditure in non-human primates". Proceedings of the Royal Society B 266 (1437): 2479–85. doi:10.1098/rspb.1999.0949. JSTOR 1353815. PMC 1690481. PMID 10693818. 
  2. ^ a b Cheverud, James M.; Dow, Malcolm M.; Leutenegger, Walter (1985). "The Quantitative Assessment of Phylogenetic Constraints in Comparative Analyses: Sexual Dimorphism in Body Weight Among Primates". Evolution 39 (6): 1335–51. doi:10.2307/2408790. JSTOR 2408790. 
  3. ^ Koppe, Thomas; Swindler, Daris R. (2004). "Metric sexual dimorphism in the deciduous teeth of old world monkeys". Annals of Anatomy - Anatomischer Anzeiger 186 (4): 367–74. doi:10.1016/S0940-9602(04)80065-7. PMID 15481844. 
  4. ^ Plavcan, J. Michael; Ruff, Christopher B. (2008). "Canine size, shape, and bending strength in primates and carnivores". American Journal of Physical Anthropology 136 (1): 65–84. doi:10.1002/ajpa.20779. PMID 18186502. 
  5. ^ Blanco, M. B.; Godfrey, L. R. (2006). "Craniofacial sexual dimorphism in Alouatta palliata, the mantled howling monkey". Journal of Zoology 270 (2): 268–76. doi:10.1111/j.1469-7998.2006.00133.x. 
  6. ^ a b Anemone, R. L.; Swindler, D. R. (1999). "Heterochrony and sexual dimorphism in the skull of the Liberian chimpanzee (Pan troglodytes verus)". International Journal of Anthropology 14 (1): 19–30. doi:10.1007/BF02447624. 
  7. ^ Dierbach, A. (1986). "Intraspecific variability and sexual dimorphism in the skulls of Pan troglodytes verus". Human Evolution 1 (1): 41–50. doi:10.1007/BF02437284. 
  8. ^ Leigh, Steven R.; Cheverud, James M. (1991). "Sexual dimorphism in the baboon facial skeleton". American Journal of Physical Anthropology 84 (2): 193–208. doi:10.1002/ajpa.1330840209. PMID 2021194. 
  9. ^ a b c d e Crook, John Hurrell (1972). "Sexual Selection, Dimorphism, and Social Organization in the Primates". In Campbell, Bernard G. Sexual Selection and the Descent of Man: The Darwinian Pivot. Chicago: Aldine. pp. 231–81. ISBN 978-0-202-02005-1. 
  10. ^ a b Marty, Jill S.; Higham, James P.; Gadsby, Elizabeth L.; Ross, Caroline (2009). "Dominance, Coloration, and Social and Sexual Behavior in Male Drills Mandrillus leucophaeus". International Journal of Primatology 30 (6): 807–23. doi:10.1007/s10764-009-9382-x. 
  11. ^ French, Jeffrey A.; Snowdon, Charles T. (1981). "Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus". Animal Behaviour 29 (3): 822–9. doi:10.1016/S0003-3472(81)80016-4. 
  12. ^ Cheney, Dorothy L.; Seyfarth, Robert M. (1983). "Nonrandom Dispersal in Free-Ranging Vervet Monkeys: Social and Genetic Consequences". The American Naturalist 122 (3): 392–412. doi:10.1086/284142. JSTOR 2461023. 
  13. ^ Kamilar, J. M.; Cooper, N. (2013). "Phylogenetic signal in primate behaviour, ecology and life history". Philosophical Transactions of the Royal Society B 368 (1618): 20120341. doi:10.1098/rstb.2012.0341. PMC 3638444. PMID 23569289. 
  14. ^ Kamilar, Jason; Pokempner, Amy (2008). "Does body mass dimorphism increase male–female dietary niche separation? A comparative study of primates". Behaviour 145 (9): 1211–4. doi:10.1163/156853908785387601. 
  15. ^ Trivers, Robert L. (1972). "Parental Investment and Sexual Selection". In Campbell, Bernard Grant. Sexual Selection and the Descent of Man: The Darwinian Pivot. Chicago: Aldine. pp. 136–79. ISBN 978-0-202-02005-1. 
  16. ^ Weir, Laura K.; Grant, James W. A.; Hutchings, Jeffrey A. (2011). "The Influence of Operational Sex Ratio on the Intensity of Competition for Mates". The American Naturalist 177 (2): 167–76. doi:10.1086/657918. PMID 21460553. 
  17. ^ a b c d Plavcan, J. Michael; Van Schaik, Carel P. (1997). "Intrasexual competition and body weight dimorphism in anthropoid primates". American Journal of Physical Anthropology 103 (1): 37–68. doi:10.1002/(SICI)1096-8644(199705)103:1<37::AID-AJPA4>3.0.CO;2-A. PMID 9185951. 
  18. ^ Pradhan, Gauri R.; Engelhardt, Antje; Schaik, Carel P.; Maestripieri, Dario (2005). "The evolution of female copulation calls in primates: A review and a new model". Behavioral Ecology and Sociobiology 59 (3): 333–43. doi:10.1007/s00265-005-0075-y. JSTOR 25063709. 
  19. ^ Daspre, Agnès; Heistermann, Michael; Hodges, J. Keith; Lee, Phyllis C.; Rosetta, Lyliane (2009). "Signals of female reproductive quality and fertility in colony-living baboons (Papio h. Anubis) in relation to ensuring paternal investment". American Journal of Primatology 71 (7): 529–38. doi:10.1002/ajp.20684. PMID 19373878. 
  20. ^ Maestripieri, Dario (2011). "Emotions, stress, and maternal motivation in primates". American Journal of Primatology 73 (6): 516–29. doi:10.1002/ajp.20882. PMID 20872879. 
  21. ^ Gordon, Adam D.; Johnson, Steig E.; Louis Jr, Edward E. (2013). "Females are the ecological sex: Sex-specific body mass ecogeography in wild sifaka populations (Propithecusspp.)". American Journal of Physical Anthropology 151 (1): 77–87. doi:10.1002/ajpa.22259. PMID 23595644. 
  22. ^ Dunham, A. E.; Rudolf, V. H. W. (2009). "Evolution of sexual size monomorphism: The influence of passive mate guarding". Journal of Evolutionary Biology 22 (7): 1376–86. doi:10.1111/j.1420-9101.2009.01768.x. PMID 19486235. 
  23. ^ Leutenegger, Walter; Cheverud, James (1982). "Correlates of sexual dimorphism in primates: Ecological and size variables". International Journal of Primatology 3 (4): 387–402. doi:10.1007/BF02693740. 
  24. ^ Muchlinski, Magdalena N.; Snodgrass, J. Josh; Terranova, Carl J. (2012). "Muscle Mass Scaling in Primates: An Energetic and Ecological Perspective". American Journal of Primatology 74 (5): 395–407. doi:10.1002/ajp.21990. PMID 22318851.