Monogamy in animals

This article is about monogamy in non-human species. For monogamy in humans, see monogamy.

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.

Animals

The evolution of mating systems in animals has received an enormous amount of attention from biologists. This section briefly reviews three main findings about the evolution of monogamy in animals.

The amount of social monogamy in animals varies across taxa, with over 90% of birds engaging in social monogamy while only 3% of mammals are known to do the same.[1][2]

This list is not complete. Other factors may also contribute to the evolution of social monogamy. Moreover, different sets of factors may explain the evolution of social monogamy in different species. There is no one-size-fits-all explanation of why different species evolved monogamous mating systems.

Sexual dimorphism

Sexual dimorphism refers to differences in body characteristics between females and males. A frequently studied type of sexual dimorphism is body size. For example among mammals, males typically have larger bodies than females. In other orders, however, females have larger bodies than males. Sexual dimorphism in body size has been linked to mating behavior.[3][4][5][6] In polygynous species, males compete for control over sexual access to females. Large males have an advantage in the competition for access to females, and they consequently pass their genes along to a greater number of offspring. This eventually leads to large differences in body size between females and males. Polygynous males are often 1.5 to 2.0 times larger in size than females. In monogamous species, on the other hand, females and males have more equal access to mates, so there is little or no sexual dimorphism in body size. From a new biological point of view, monogamy could result from mate guarding and is engaged as a result of sexual conflict.[7]

Some researchers have attempted to infer the evolution of human mating systems from the evolution of sexual dimorphism. Several studies have reported a large amount of sexual dimorphism in Australopithecus, an evolutionary ancestor of human beings that lived between 2 and 5 million years ago.[4][5][8][9] These studies raise the possibility that Australopithecus had a polygamous mating system. Sexual dimorphism then began to decrease. Studies suggest sexual dimorphism reached modern human levels around the time of Homo erectus 0.5 to 2 million years ago.[4][5][8][10] This line of reasoning suggests human ancestors started out polygamous and began the transition to monogamy somewhere between 0.5 million and 2 million years ago.

Attempts to infer the evolution of monogamy based on sexual dimorphism remain controversial for three reasons:

  • The skeletal remains of Australopithecus are quite fragmentary. This makes it difficult to identify the sex of the fossils. Researchers sometimes identify the sex of the fossils by their size, which, of course, can exaggerate findings of sexual dimorphism.
  • Recent studies using new methods of measurement suggest Australopithecus had the same amount of sexual dimorphism as modern humans.[11][12] This raises questions about the amount of sexual dimorphism in Australopithecus.
  • Humans may have been partially unique in that selection pressures for sexual dimorphism might have been related to the new niches that humans were entering at the time, and how that might have interacted with potential early cultures and tool use. If these early humans had a differentiation of gender roles, with men hunting and women gathering, selection pressures in favor of increased size may have been distributed unequally between the sexes.
  • Even if future studies clearly establish sexual dimorphism in Australopithecus, other studies have shown the relationship between sexual dimorphism and mating system is unreliable.[3][4] Some polygamous species show little or no sexual dimorphism. Some monogamous species show a large amount of sexual dimorphism.

Studies of sexual dimorphism raise the possibility that early human ancestors were polygamous rather than monogamous. But this line of research remains highly controversial. It may be that early human ancestors showed little sexual dimorphism, and it may be that sexual dimorphism in early human ancestors had no relationship to their mating systems.

Testis size

Chimpanzee
Male and female gorilla

The relative sizes of male testes often reflect mating systems.[13][14][15][16] In species with promiscuous mating systems, where many males mate with many females, the testes tend to be relatively large. This appears to be the result of sperm competition. Males with large testes produce more sperm and thereby gain an advantage impregnating females. In polygynous species, where one male controls sexual access to females, the testes tend to be small. One male defends exclusive sexual access to a group of females and thereby eliminates sperm competition.

Studies of primates, including humans, support the relationship between testis size and mating system.[15][16][17] Chimpanzees, which have a promiscuous mating system, have large testes compared to other primates. Gorillas, which have a polygynous mating system, have smaller testes than other primates. Humans, which have a socially monogamous mating system, accompanied by moderate amounts of sexual non-monogamy (see incidence of monogamy), have moderately sized testes. The moderate amounts of sexual non-monogamy in humans may result in a low to moderate amount of sperm competition. Also, notably, in the case of an avowedly sexually monogamous society, the occurrence of sexual nonmonogamy is typically culturally stigmatized, and therefore detecting its prevalence is inherently difficult, if indeed it is at all possible. At best, such statistics can be viewed as general approximations with a wide margin of error.

Monogamy as a best response

In species where the young are particularly vulnerable and may benefit from protection by both parents, monogamy may be an optimal strategy. Monogamy tends to also occur when populations are small and dispersed. This is not conductive to polygamous behavior as the male would spend far more time searching for another mate. The monogamous behavior allows the male to have a mate consistently, without having to waste energy searching for other females. Furthermore, there is an apparent connection between the time a male invests in their offspring and their monogamous behavior. A male which is required to care for the offspring to ensure their survival is much more likely to exhibit monogamous behavior over one that does not. The selection factors in favor of different mating strategies for a species of animal, however, may potentially operate on a large number of factors throughout that animal's life cycle. For instance, with many species of bear, the female will often drive a male off soon after mating, and will later guard her cubs from him. It is thought that this may be due to the fact that too many bears close to one another may deplete the food available to the relatively small but growing cubs. Monogamy may be social but rarely genetic. For example, in the cichlid species Variabilichromis moorii, a monogamous pair will care for their eggs and young but the eggs are not all fertilized by the same male.[18] Thierry Lodé[19] argued that monogamy should result from conflict of interest between the sexes called sexual conflict.

Monogamous species

While it is difficult to find monogamous relationships in nature, there are a few species which have adopted monogamy with great success. For instance, the prairie vole will mate exclusively with the first female he ever mates with. The vole is extremely loyal and will go as far as to even attack other females that may approach him. This type of behavior has been linked to the hormone vasopressin. This hormone is released when a male mates and cares for young. Due to this hormone's rewarding effects, the male experiences a positive feeling when they maintain a monogamous relationship. To further test this theory, the receptors that control vasopressin were placed into another species of vole that is promiscuous. After this addition, the originally unfaithful voles became monogamous with their selected partner. These very same receptors can be found in human brain, and have been found to vary at the individual level -- which could explain why some human males tend to be more loyal than others. [20][21][22]

Black vultures stay together as it is more beneficial for their young to be taken care of by both parents. They take turns incubating the eggs, and then supplying their fledglings with food. Black vultures will also attack other vultures that are participating in extra pair copulation, this is an attempt to increase monogamy and decrease promiscuous behavior. [23] Similarly, emperor penguins also stay together to care for their young. This is due to the harshness of the arctic weather, predators and the scarcity of food. One parent will protect the chick, while the other finds food. However, these penguins only remain monogamous until the chick is able to go off on their own. After the chick no longer needs their care, approximately 85% of parents will part ways and typically find a new partner every breeding season.

Hornbills are a socially monogamous bird species that usually only have one mate throughout their lives, much like the prairie vole. The females will close herself up in a nest cavity, sealed with a nest plug, for two months. At this time, she will lay eggs and will be cared for by her mate. The males are willing to work to support himself, his mate, and his offspring in order for survival. However, unlike the emperor penguin, the hornbills do not find new partners each season. [24]

It is relatively uncommon to find monogamous relationships in fish, amphibians and reptiles. However, the red back salamander as well as the Caribbean cleaner goby practice monogamy as well. However, the male Caribbean cleaner goby fish has been found to separate from the female suddenly, leaving her abandoned. In a study conducted by Oregon State University, it was found that this fish practices not true monogamy, but serial monogamy. This essentially means that the goby will have multiple monogamous relationships throughout its life - but only be in one relationship at a time. [25] The red backed salamander exhibited signs of social monogamy, which is the idea that animals form pairs to mate and raise offspring, but still will partake in extra pair copulation with various males or females in order to increase their biological fitness. This is relatively new concept in salamanders, and has not been seen frequently - it is also concerning that the act of monogamy may inhibit the salamanders reproductive rates and biological success. However, the study which was conducted in cooperation by the University of Louisiana, Lafayette, and the University of Virginia showed that the salamanders are not inhibited by this monogamy if they show alternative strategies with other mates. [26]

Azara's owl monkeys are another species that proved to be monogamous. In an 18 year study conducted by the University of Pennsylvania, these monkeys proved to be entirely monogamous, exhibiting no genetic information or visual information that could lead to the assumption that extra pair copulation was occurring. This explained the question as to why the male owl monkey invested so much time in protecting and raising their own offspring. Because monogamy if often referred to "placing all your eggs in one basket" the male wants to ensure his young survive, and thus pass on his genes. [27]

Other monogamous species include wolves, otters, a few hooved animals, some bats, certain species of fox and the European beaver. This beaver is particularly interesting as it is practicing monogamy in its reintroduction to certain parts of Europe. Its' American counterpart, however is not monogamous at all and often partakes in promiscuous behavior. The two species are quite similar in ecology but American beavers tend to be less aggressive than European beavers. In this instance, the European beavers' population is scarce. This could attribute to its monogamous behavior. Moreover, it lowers the risk of parasite transmission which is correlated with biological fitness. Monogamy is proving to be very efficient for this beaver, as their population is climbing. [28]

See also

Monogamy topics:

Evolution topics:

References

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  2. Barash, D.P. & Lipton, J.E. (2001). The Myth of Monogamy. New York, NY: W.H. Freeman and Company.
  3. 1 2 Owens, I.P.F. & Hartley, I.R. (1998). "Sexual dimorphism in birds: why are there so many different forms of dimorphism?" Proceedings of the Royal Society of London B, 265, 397-407.
  4. 1 2 3 4 Frayer, D.W. & Wolpoff, M.H. (1985). "Sexual dimorphism". Annual Review of Anthropology, 14, 429-473.
  5. 1 2 3 Geary, D.C., & Flinn, M.V. (2001). "Evolution of human parental behavior and the human family". Parenting: Science and Practice, 1, 5-61.
  6. Dunn, P.O., Whittingham, L.A., & Pitcher, T.E. (2001). "Mating systems, sperm competition, and the evolution of sexual dimorphism in birds". Evolution, 55, 161–175.
  7. T Lodé “la guerre des sexes chez les animaux” Eds O Jacob, Paris, 2006, ISBN 2-7381-1901-8
  8. 1 2 Flinn, M.V. & Ward, C.V. (2004). "Ontogeny and Evolution of the Social Child". In: Origins of the social mind: Evolutionary psychology and child development, B. Ellis & D. Bjorklund (Eds.), chapter 2, pp. 19-44. London: Guilford Press.
  9. Lockwood, C.A., Richmond, B.G., Jungers, W.L., & Kimbel, W.H. (1996). "Randomization procedures and sexual dimorphism in Australopithecus afarensis". Journal of Human Evolution, 31, 537-548.
  10. Arsuaga, J.L., Carretero, J.M., Lorenzo, C., Gracia, A., Martínez, I., Bermúdez de Castro, J.M., & Carbonell, E. (1997). "Size variation in Middle Pleistocene humans". Science, 277, 1086-1088.
  11. Reno, P.L., Meindl, R.S., McCollum, M.A., & Lovejoy, C.O. (2003). "Sexual dimorphism in Australopithecus afarensis was similar to that of modern humans". Proceedings of the National Academy of Sciences, 100, 9404-9409.
  12. Larsen, C.S. (2003). "Equality for the sexes in human evolution? Early hominid sexual dimorphism and implications for mating systems and social behavior". Proceedings of the National Academy of Sciences, 100, 9103-9104.
  13. Pitcher, T.E., Dunn, P.O., & Whittingham, L.A. (2005). "Sperm competition and the evolution of testes size in birds". Journal of Evolutionary Biology, 18, 557–567.
  14. Simmons, L.W., Firman, R.E.C., Rhodes, G., & Peters, M. (2004). "Human sperm competition: testis size, sperm production and rates of extrapair copulations". Animal Behaviour, 68, 297-302.
  15. 1 2 Dixson, A., & Anderson, M. (2001). "Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings". Annual Review of Sex Research, 12, 121-144.
  16. 1 2 Harcourt, A.H., Harvey, P.H., Larson, S.G., & Short, R.V. (1981). "Testis weight, body weight and breeding system in primates". Nature, 293, 55-57.
  17. T. R. Birkhead (2000), Promiscuity: an evolutionary history of sperm competition. Harvard University Press, Cambridge, Mass.
  18. Sefc, Kristina M.; Karin Mattersdorfer; Christian Sturmbauer; Stephan Koblmüller (2008). "High Frequency of Multiple Paternity in Broods of a Socially Monogamous Cichlid Fish with Biparental Nest Defence". Molecular Ecology 17 (10): 2531–2543. doi:10.1111/j.1365-294x.2008.03763.x. Retrieved 30 September 2013.
  19. Thierry Lodé "La Guerre des sexes chez les animaux" Eds O Jacob, Paris, 2006
  20. http://www.nsf.gov/discoveries/disc_summ.jsp?cntn_id=126932
  21. Alcock, J. (2009). Animal behavior: An evolutionary approach (9th ed.). Sunderland, Mass.: Sinauer Associates.
  22. Ophir, A. G., Phelps, S. M., Sorin, A. B., & Wolff, J. O. (2008). Social but not genetic monogamy is associated with greater breeding success in prairie voles. Animal Behaviour, 751143-1154. doi:10.1016/j.anbehav.2007.09.022
  23. http://www.nsf.gov/discoveries/disc_summ.jsp?cntn_id=126932
  24. Stanback, M., Richardson, D. S., Boix-Hinzen, C., & Mendelsohn, J. (2002). Regular Articles: Genetic monogamy in Monteiro's hornbill, Tockus monteiri. Animal Behaviour, 63787-793. doi:10.1006/anbe.2001.1975
  25. Harding, J. A., Almany, G. R., Houck, L. D., & Hixon, M. A. (2003). Regular Articles: Experimental analysis of monogamy in the Caribbean cleaner goby, Gobiosoma evelynae. Animal Behaviour, 65865-874. doi:10.1006/anbe.2003.2144
  26. Gillette, J. R., Jaeger, R. G., & Peterson, M. G. (2000). Regular Article: Social monogamy in a territorial salamander. Animal Behaviour, 591241-1250. doi:10.1006/anbe.2000.1437
  27. Huck, M., Fernandez-Duque, E., Babb, P., & Schurr, T. (2014). Correlates of genetic monogamy in socially monogamous mammals: Insights from Azara's owl monkeys. Proceedings B, 281(1782).
  28. Herr, J., & Rosell, F. (2004). Use of space and movement patterns in monogamous adult Eurasian beavers. Journal of Zoology, 262(03).

Bibliography

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