Extra-pair copulation (EPC) is a promiscuous mating behaviour in monogamous species. Monogamy occurs when an individual has only one sexual partner at any one time, forming a long term bond and combining efforts to raise offspring together; extra-pair copulation occurs when one of these individuals mates outside of this pairing. Across the animal kingdom, extra-pair copulation is common in monogamous species, and only a very few pair-bonded species are thought to be exclusively sexually monogamous. EPC in the animal kingdom has mostly been studied in birds and mammals. Possible benefits of EPC can be investigated within non-human species, such as birds. In males, a number of theories are proposed to explain extra-pair copulations. One such hypothesis is that males maximise their reproductive success by copulating with as many females as possible outside of a pair bond relationship because their parental investment is lower, meaning they can copulate and leave the female with minimum risk to themselves. Females, on the other hand, have to invest a lot more in their offspring; extra-pair copulations produce a greater cost because they put the resources that their mate can offer at risk by copulating outside the relationship. Despite this, females do seek out extra pair copulations, and, because of the risk, there is more debate about the evolutionary benefits for females.
Extra-pair copulation in men has been explained as being partly due to parental investment. Research has suggested that copulation poses more of a risk to future investment for women, as they have the potential of becoming pregnant, and consequently require a large parental investment of the gestation period, and then further rearing of the offspring. Contrastingly, men are able to copulate and then abandon their mate as there is no risk of pregnancy for themselves, meaning there is a smaller risk of parental investment in any possible offspring. It has been suggested that, due to having such low parental investment, it is evolutionarily adaptive for men to copulate with as many women as possible, as it will allow them to spread their genes with little risk of future investment. This may therefore lead to more extra-pair copulation in men, as they are able to copulate with other women without the consequences of having to rear new offspring.
Various factors can increase the probability of EPC in males. Firstly, males with low levels of fluctuating asymmetry are more likely to have EPCs. This may be due to the fact that signals of low fluctuating asymmetry suggest that the males have "good genes", making females more likely to copulate with them as it will enhance the genes of their offspring, even if they do not expect long term commitment from the male. Psychosocial stress early on in life, including behaviours such as physical violence and substance abuse, can predict EPC in later life. This has been explained as being due to Life History Theory, which argues that individuals who are reared in environments, where resources are scarce and life expectancy is low, are more likely to engage in reproductive behaviours earlier in life in order to ensure the proliferation of their genes. Individuals reared in these environments are said to have short life histories. With respect to Life History Theory, these finding have been explained by suggesting that males who experienced psychosocial stress early in life have short life histories, making them more likely to try and reproduce as much as possible by engaging in EPC to avoid gene extinction.
However, men may also choose not to have EPCs for multiple reasons. One reason may be that long-term monogamous relationships can help form environments that will aid the successful rearing of offspring, as the male is present to help raise them, leading to an increased probability of the male's genes surviving to the next generation. A second reason that ECP may be avoided by a male is that it can be costly to them; their EPC may be discovered, leading to the dissolution of the long-term relationship with their partner and, in some cases, lead to their partner assaulting or even killing them. Men may also avoid EPCs to minimize the risk of putting themselves at increased opportunity for STD transmission which can be common in EPCs. The partners in the EPC may be promiscuous as well leading to a higher statistical chance and probability of contracting venereal diseases; this would counter the lower incidence of STD transmission among exclusively monogamous sexually active couples. Spousal homicide is more likely to be committed by males rather than females, which may make the ramifications of EPC more relevant to women.
From an evolutionary perspective, females have to invest a lot more in their offspring than males due to prolonged pregnancy and child rearing, and a child has a better chance of survival and development with two parents involved in child-rearing. Therefore, extra-pair copulations have a greater cost for women because they put the support and resources that their mate can offer at risk by copulating outside the relationship. There is also the increased risk of sexually transmitted infections which is suggested as a possible evolutionary reason for the transition from polygamous to monogamous relationships in humans. Despite this, females do seek out extra-pair copulation, with some research finding that women's levels of infidelity are equal to that of men's, although this evidence is mixed. Due to the increased risk, there is more confusion about the evolutionary benefits of extra-pair copulation for females.
The most common theory is that women mate outside of the monogamous relationship to acquire better genetic material for their offspring. A female in a relationship with a male with 'poorer genetic quality' may try to enhance the fitness of her children and therefore the continuation of her own genes by engaging in extra-pair copulation with better quality males. A second theory is that a woman will engage in extra-pair copulation to seek additional resources for herself or her offspring. This is based on observations from the animal world in which females may copulate outside of their pair-bond relationship with neighbours to gain extra protection, food or nesting materials. Finally, evolutionary psychologists have theorized that extra-pair copulation is an indirect result of selection on males. The alleles in males that promote extra-pair copulation as an evolutionary strategy to increase reproductive success is shared between sexes leading to this behaviour being expressed in females.
There are also social factors involved in extra-pair copulation. Both males and females have been found to engage in more sexual behaviour outside of the monogamous relationship when experiencing sexual dissatisfaction in the relationship, although how this links to evolutionary theory is unclear. Surveys have found cultural differences in attitudes towards infidelity, though it is relatively consistent that female attitudes are less favorable toward infidelity than male attitudes.
As well as humans, EPC has been found in many other socially monogamous species.
When EPC occurs in animals which show sustained female-male social bonding, this can lead to extra-pair paternity (EPP), in which the female reproduces with an extra-pair male, and hence produces EPO (extra-pair offspring).
Due to the obvious reproductive success benefits for males, it used to be thought that males exclusively controlled EPCs. However, it is now known that females also seek EPC in some situations.
Extra-pair copulation is common in birds. For example, zebra finches, although socially monogamous, are not sexually monogamous and hence do engage in extra-pair courtship and attempts at copulation. In a laboratory study, female zebra finches copulated over several days, many times with one male and only once with another male. Results found that significantly more eggs were fertilised by the extra-pair male than expected proportionally from just one copulation verses many copulations with the other male. EPO proportion varies between different species of birds. For example, in eastern bluebirds, studies have shown that around 35% of offspring is due to EPC.
In socially polygynous birds, EPP is only half as common as in socially monogamous birds. Some ethologists consider this finding to be support for the 'female choice' hypothesis of mating systems in birds.
Additionally, EPC has been shown in monogamous mammals, such as the white-handed gibbon. A study of one group found 88% in-pair copulation and 12% extra-pair copulation. However, there is much variability in rates of EPP in mammals. One study found that this disparity in EPP is better predicted by the differing social structures of different mammals, rather than differing types of pair bonding. For example, EPP was lower in species who live in pairs compared to those who live in solitary or family structures.
Reasons for evolution
Some argue that EPC is one way in which sexual selection is operating for genetic benefits which is why the extra-pair males involved in EPC seem to be a non-random subset. There is some evidence for this in birds. For example, in swallows, males with longer tails are involved in EPC more than those with shorter tails. Also female swallows with a shorter-tailed within-pair mates are more likely to conduct EPC than those whose mates have longer tails. A similar pattern has been found for black-capped chickadees, in which all extra-pair males had higher rank than the within-pair males. But some argue that genetic benefits for offspring is not the reason females participate in EPC. A meta-analysis of genetic benefits of EPC in 55 bird species found that extra-pair offspring were not more likely to survive than within-pair offspring. Also, extra-pair males did not show significantly better ‘good-genes’ traits than within-pair males, except for being slightly larger overall.
Another potential explanation for the occurrence of EPC in organisms where females solicit EPC is that the alleles controlling such behaviour are intersexually pleiotropic. Under the hypothesis of intersexual antagonistic pleiotropy, the benefit males get from EPC cancels out the negative effects of EPC for females. Thus, the allele that controls EPC in both organisms would persist, even if it would be detrimental to the fitness of females. Similarly, according to the hypothesis of intrasexual antagonistic pleiotropy, the allele that controls EPC in females also controls a behaviour that is under positive selection, such as receptiveness towards within-pair copulation.
- Petrie, Marion; Kempenaers, Bart (1998-02-01). "Extra-pair paternity in birds: explaining variation between species and populations". Trends in Ecology & Evolution. 13 (2): 52–58. doi:10.1016/S0169-5347(97)01232-9. ISSN 0169-5347. PMID 21238200.
- Houtman, A. M. (1992-07-22). "Female Zebra Finches Choose Extra-Pair Copulations with Genetically Attractive Males". Proceedings of the Royal Society B: Biological Sciences. 249 (1324): 3–6. doi:10.1098/rspb.1992.0075.
- Gowaty, P. A.; Bridges, W. C. (1991). "Behavioral, demographic, and environmental correlates of extrapair fertilizations in eastern bluebirds". Behavioral Ecology. 2 (4): 339–350. doi:10.1093/beheco/2.4.339.
- Bollinger, E. K.; Gavin, T. A. (1991). "Patterns of extra-pair fertilizations in bobolinks". Behavioral Ecology and Sociobiology. 29 (1): 1–7. doi:10.1007/BF00164288.
- Akçay, E.; Roughgarden, J. (2007). "Extra-pair paternity in birds: Review of the genetic benefits". Evolutionary Ecology Research. 9 (5).
- Forstmeier, Wolfgang; Martin, Katrin; Bolund, Elisabeth; Schielzeth, Holger; Kempenaers, Bart (2011-06-28). "Female extrapair mating behavior can evolve via indirect selection on males". Proceedings of the National Academy of Sciences. 108 (26): 10608–10613. doi:10.1073/pnas.1103195108. ISSN 0027-8424. PMC 3127899. PMID 21670288.
- Buss, David M (1989). "Sex differences in human mate preferences: Evolutionary hypotheses tested in 37 cultures". Behavioral and Brain Sciences. 12 (1): 1–49. doi:10.1017/S0140525X00023992.
- Trivers, Robert (1996). Parental investment and sexual selection (PDF). University of Chicago Press. pp. 795–838. ISBN 0-226-35456-3.
- Trivers, Robert (1996). Parental investment and sexual selection (PDF). University of Chicago Press. pp. 795–838. ISBN 0-226-35456-3.
- Gangestad, Steven; Simpson, Jeffry (2000). "The evolution of human mating: Trade-offs and strategic pluralism". Behavioral and Brain Sciences. 23 (4): 573–644. doi:10.1017/S0140525X0000337X. PMID 11301543.
- Gangestad, Steven W; Thornhill, Randy (1997). "The evolutionary psychology of extrapair sex: The role of fluctuating asymmetry". Evolution and Human Behavior. 18 (2): 69–88. doi:10.1016/S1090-5138(97)00003-2.
- Koehler, Nicole; Chisholm, James S (2007). "Early Psychosocial Stress Predicts Extra-pair Copulations". Evolutionary Psychology. 5 (1): 184–201. doi:10.1177/147470490700500111.
- Kaplan, Hillard S; Gangestad, Steven W (2005). Life History Theory and Evolutionary Psychology. John Wiley & Sons Inc (Hoboken, NJ, US). pp. 68–95. ISBN 0471264032.
- Mellen, Sydney (1981). The Evolution of Love. Oxford: WH Freeman. p. 312. ISBN 0716712717.
- Daly, Martin; Wilson, Margo (1988). Homicide. Aldine de Gruyter (Hawthorne, NY, US). p. 328. ISBN 0202011771.
- Morell, Virginia (1998-09-25). "A New Look at Monogamy". Science. 281 (5385): 1982–1983. doi:10.1126/science.281.5385.1982. ISSN 0036-8075. PMID 9767050.
- Bauch, Chris T.; McElreath, Richard (2016-04-12). "Disease dynamics and costly punishment can foster socially imposed monogamy". Nature Communications. 7: 11219. doi:10.1038/ncomms11219. PMC 4832056. PMID 27044573.
- Buss, David M.; Shackelford, Todd K. (1997-06-01). "Susceptibility to Infidelity in the First Year of Marriage". Journal of Research in Personality. 31 (2): 193–221. doi:10.1006/jrpe.1997.2175.
- CHRISTENSEN, HAROLD T. (1973-01-01). "Attitudes Toward Marital Infidelity: A Nine-Culture Sampling of University Student Opinion". Journal of Comparative Family Studies. 4 (2): 197–214. JSTOR 41600842.
- Evarts, S.; Williams, C.J. (1987). "Multiple paternity in a wild population of Mallards". The Auk. 104 (4): 597–602. JSTOR 4087269.
- Sherman, P.W.; Morton, M.L. (1988). "Extra-pair fertilizations in mountain white-crowned sparrows". Behavioral Ecology and Sociobiology. 22 (6): 413–420. doi:10.1007/BF00294979.
- Reichard, U. (1995). "Extra-pair Copulations in a Monogamous Gibbon (Hylobates lar)". Ethology. 100 (2): 99–112. doi:10.1111/j.1439-0310.1995.tb00319.x.
- Crawford, J.C.; Liu, Z.; Nelson, T.A.; Nielsen, C.K.; Bloomquist, C.K. (2008). "Microsatellite analysis of mating and kinship in beavers (Castor canadensis)". Journal of Mammalogy. 89 (3): 575–581. doi:10.1644/07-MAMM-A-251R1.1.
- Bishop, J.M.; Jarvis, J.U.M.; Spinks, A.C.; Bennett, N.C.; O'Ryan, C. (2004-03-31). "Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus". Molecular Ecology. 13 (5): 1217–1229. doi:10.1111/j.1365-294X.2004.02131.x. PMID 15078457.
- Baker, P.J.; Funk, S.M.; Bruford, M.W.; Harris, S. (2004-06-11). "Polygynandry in a red fox population: implications for the evolution of group living in canids?". Behavioral Ecology. 15 (5): 766–778. doi:10.1093/beheco/arh077.
- Kitchen, A.M.; Gese, E.M.; Waits, L.P.; Karki, S.M.; Schauster, E.R. (2006). "Multiple breeding strategies in the swift fox, Vulpes velox". Animal Behaviour. 71 (5): 1029–1038. doi:10.1016/j.anbehav.2005.06.015.
- Young, A.J; Spong, G.; Clutton-Brock, T. (2007-07-07). "Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal". Proceedings of the Royal Society B: Biological Sciences. 274 (1618): 1603–1609. doi:10.1098/rspb.2007.0316. PMC 2169281. PMID 17456454.
- Gowaty, P.A. (2006). "Beyond extra-pair paternity". In Lucas, Jeffrey; Simmons, Leigh. Essays in animal behaviour: Celebrating 50 years of animal behaviour. Burlington, MA: Elsevier Academic Press. pp. 221–254. ISBN 0-12-369499-X.
- Welty, J.C.; Baptista, L.F. (1988). The life of birds (4th ed.). New York: Saunders College Pub. ISBN 0-03-068923-6.
- Birkhead, T.; Parker, G. (1996). "Sperm competition and mating systems". In Krebs, John; Davies, Nicholas. Behavioural ecology: an evolutionary approach (4th ed.). Cambridge: Blackwell Science. pp. 121–145. ISBN 0-86542-731-3.
- Birkhead, T. R.; Pellatt, J.; Hunter, F. M. (1988). "Extra-pair copulation and sperm competition in the zebra finch". Nature. 334 (6177): 60–62. doi:10.1038/334060a0.
- Petrie, M.; Kempenaers, B. (1998). "Extra-pair paternity in birds: explaining variation between species and populations". Trends in Ecology & Evolution. 13 (2): 52–58. doi:10.1016/S0169-5347(97)01232-9. PMID 21238200.
- Hasselquist, D.; Sherman, P. (2001). "Social mating systems and extrapair fertilizations in passerine birds". Behavioral Ecology. 12 (4): 457–466. doi:10.1093/beheco/12.4.457.
- Palombit, Ryne A. (1994). "Extra-pair copulations in a monogamous ape" (PDF). Animal Behaviour. 47 (3): 721–723. doi:10.1006/anbe.1994.1097.
- Cohas, A.; Allaine, D. (2009-03-04). "Social structure influences extra-pair paternity in socially monogamous mammals". Biology Letters. 5 (3): 313–316. doi:10.1098/rsbl.2008.0760. PMC 2679913. PMID 19324647.
- Gray, E.M. (1997). "Do female red-winged blackbirds benefit genetically from seeking extra-pair copulations?". Animal Behaviour. 53 (3): 605–623. doi:10.1006/anbe.1996.0337.
- Møller, A.P. (1988-04-14). "Female choice selects for male sexual tail ornaments in the monogamous swallow". Nature. 332 (6165): 640–642. doi:10.1038/332640a0.
- Smith, S.M. (1988-01-01). "Extra-Pair Copulations in Black-Capped Chickadees: the Role of the Female". Behaviour. 107 (1): 15–23. doi:10.1163/156853988X00160.
- Forstmeier, Wolfgang; Nakagawa, Shinichi; Griffith, Simon C.; Kempenaers, Bart (2014). "Female extra-pair mating: adaptation or genetic constraint?". Trends in Ecology & Evolution. 29 (8): 456–464. doi:10.1016/j.tree.2014.05.005. ISSN 0169-5347.