extra-pair copulation
{{short description|Non-monogamy in monogamous species}}
{{use dmy dates|date=February 2025}}
Extra-pair copulation (EPC) is a mating behaviour in monogamous species. Monogamy is the practice of having only one sexual partner at any one time, forming a long-term bond and combining efforts to raise offspring together; mating outside this pairing is extra-pair copulation.{{Cite journal|last1= Petrie|first1= Marion |last2=Kempenaers|first2=Bart|date=February 1998 |title=Extra-pair paternity in birds: explaining variation between species and populations|journal=Trends in Ecology & Evolution|language=English|volume=13|issue=2|pages=52–58|doi=10.1016/S0169-5347(97)01232-9|issn=0169-5347|pmid=21238200|bibcode=1998TEcoE..13...52P }} 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.{{r|Houtman, 1992|Gowaty and Bridges 1991a|bollinger and gavin, 1991}} Possible benefits of EPC can be investigated within non-human species, such as birds.
For 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.{{r|Petrie 1998}} Despite this, females do seek out extra pair copulations,{{r|forstmeier 2011}} and, because of the risk, there is more debate about the evolutionary benefits for females.
In human males
Extra-pair copulation in men has been explained as being partly due to parental investment.{{cite journal |last1=Buss|first1=David M.|title=Sex differences in human mate preferences: Evolutionary hypotheses tested in 37 cultures |journal=Behavioral and Brain Sciences |date=1989|volume=12|issue=1|pages=1–49|doi=10.1017/S0140525X00023992|doi-access=free}} 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.{{r|buss 1989}} 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.{{cite book |last1=Trivers |first1=Robert |title=Parental investment and sexual selection |date=1996 |publisher= University of Chicago Press |isbn=978-0-226-35456-9 |pages=795–838 |access-date=2016-03-02 |url-status=dead |url=http://www1.appstate.edu/~kms/classes/psy2664/Documents/trivers.pdf |archive-date=2016-03-04 |archive-url=https://web.archive.org/web/20160304025739/http://www1.appstate.edu/~kms/classes/psy2664/Documents/trivers.pdf }} It has been suggested that,{{r|trivers}} due to having such low parental investment, it is evolutionarily adaptive for men to copulate with as many women as possible. This will allow males to spread their genes with little risk of future investment but it does come with the increased risk of sexually transmitted infections (STIs).{{cite journal |last1=Gangestad |first1=Steven |last2=Simpson |first2=Jeffry |title=The evolution of human mating: Trade-offs and strategic pluralism |journal=Behavioral and Brain Sciences |date=2000 |volume=23 |issue=4 |pages=573–644 |url-access=subscription |doi=10.1017/S0140525X0000337X |pmid=11301543 |s2cid=33245508 |url=http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=65461&fileId=S0140525X0000337X |url-status=live |access-date=2016-03-02 |archive-date=2016-03-07 |archive-url=https://web.archive.org/web/20160307214101/http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=65461&fileId=S0140525X0000337X }}
Various factors can increase the probability of EPC in males. Firstly, males with low levels of fluctuating asymmetry are more likely to have EPCs.{{cite journal|last1=Gangestad|first1=Steven W. |last2=Thornhill |first2=Randy |title=The evolutionary psychology of extrapair sex: The role of fluctuating asymmetry |journal=Evolution and Human Behavior |date=1997 |volume=18 |issue=2|pages=69–88 |doi=10.1016/S1090-5138(97)00003-2|bibcode=1997EHumB..18...69G }} 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.{{r|gangestad}} Psychosocial stress early on in life, including behaviours such as physical violence and substance abuse, can predict EPC in later life.{{r|koehler 2007}} 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.{{cite book |last1=Kaplan |first1=Hillard S. |last2=Gangestad |first2=Steven W. |title=Life History Theory and Evolutionary Psychology |date=2005 |publisher=John Wiley & Sons |location=Hoboken, New Jersey US |isbn=978-0471264033|pages=68–95}} Individuals reared in these environments are said to have short life histories. With respect to Life History Theory, these findings 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.{{cite journal|last1=Koehler|first1=Nicole|last2=Chisholm|first2=James S|title=Early Psychosocial Stress Predicts Extra-pair Copulations|journal=Evolutionary Psychology|date=2007|volume=5|issue=1|pages=184–201 |doi-access=free |doi=10.1177/147470490700500111 |hdl=10536/DRO/DU:30062082|hdl-access=free|quote=Bearing in mind that both men and women can benefit by engaging in EPCs raises the question as to why more individuals do not engage in such behavior.{{nbsp}}... In the case of EPCs individuals are faced with the cost of being discovered by their pair-bonded mate which could lead to the dissolution of their relationship or in extreme cases could lead to spousal homicide because of sexual jealously, which is more commonly inflicted by men than women.}}
Despite the possibility of increased reproductive success resulting from EPC, there are risks associated with the behavior. For example, costs may include discovery of sexual behavior outside the pair bond, with the risk of breakdown of the relationship with a long-term partner; in some cases, a discovered EPC leads to violence from partners.{{r|koehler 2007}}{{efn|name="IPV"}} Men may also refrain from EPC to minimize risk of STI transmission which can be common in EPCs. The extra-pair partners in the EPC may have a higher number of sexual partners and therefore be at greater risk of STIs; this would counter the lower incidence of STI transmission among sexually exclusive, monogamous couples. Mitigating against improved reproductive success from EPC is the loss of enhanced child-rearing environments for any resulting offspring. In an evolutionary context, long-term pair-bonded couples would have greater success rearing children, increasing survival rates; offspring from EPC may have a reduced chance of survival in the absence of cooperative child-rearing from both parents, reducing the probability of the male's genes surviving to the next generation.{{cite book |last1=Mellen |first1=Sydney |title=The Evolution of Love |date=1981 |publisher=W.H. Freeman |location=Oxford |isbn=978-0716712718 |pages=[https://archive.org/details/evolutionoflove00mellrich/page/312 312] |url-access=registration |url= https://archive.org/details/evolutionoflove00mellrich/page/312}}
In human females
From an evolutionary perspective, females have to invest a lot more in their offspring than males due to prolonged pregnancy and child rearing; a child has a better chance of survival and development with two parents involved in child-rearing.{{Cite journal|last=Morell|first=Virginia|date=1998-09-25|title=A New Look at Monogamy |journal=Science |language=en |volume=281|issue=5385|pages=1982–1983|doi=10.1126/science.281.5385.1982|issn=0036-8075 |pmid=9767050 |s2cid= 31391458}} 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.{{r|Petrie 1998}} There is also the increased risk of sexually transmitted infections,{{r|Petrie 1998}} which is suggested as a possible evolutionary reason for the transition from polygamous to monogamous relationships in humans.{{Cite journal|last1=Bauch|first1=Chris T. |last2= McElreath |first2= Richard |date=2016-04-12 |title=Disease dynamics and costly punishment can foster socially imposed monogamy |journal=Nature Communications |language=en |volume=7 |pages=11219 |doi=10.1038/ncomms11219 |pmid=27044573 |pmc=4832056 |bibcode= 2016NatCo...711219B }} 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.{{Cite journal|last1=Buss|first1=David M. |last2=Shackelford|first2=Todd K.|date=June 1997|title=Susceptibility to Infidelity in the First Year of Marriage |journal= Journal of Research in Personality|volume=31|issue=2|pages=193–221|doi=10.1006/jrpe.1997.2175}} 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.{{r|morell 1998}} A second theory is that a woman will engage in extra-pair copulation to seek additional resources for herself or her offspring.{{r|Petrie 1998}} 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.{{Cite journal |last1= Forstmeier|first1=Wolfgang|last2=Martin|first2=Katrin|last3=Bolund|first3=Elisabeth|last4=Schielzeth|first4=Holger|last5=Kempenaers |first5=Bart |date=2011-06-28 |title=Female extrapair mating behavior can evolve via indirect selection on males |journal =Proceedings of the National Academy of Sciences |language=en|volume=108|issue=26 |pages=10608–10613 |doi=10.1073/pnas.1103195108 |issn=0027-8424|pmc=3127899|pmid=21670288 |doi-access=free}}
There are also social factors affecting the likelihood of 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,{{r|1997 buss Shackel}} 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. For women, the social costs of EPC may be greater, including higher levels of social disapprobation. This has a range of consequences, depending on cultural and personal circumstances. Known or suspected EPC by women may result in lowered life chances for any offspring, or the woman being at higher risk of violence and homicide, for example.{{efn|name="IPV"}}{{Cite journal |last=Christensen |first=Harold T.|date=Autumn 1973 |title=Attitudes Toward Marital Infidelity: A Nine-Culture Sampling of University Student Opinion |jstor=41600842 |journal=Journal of Comparative Family Studies |volume=4 |issue=2 |pages=197–214 |doi=10.3138/jcfs.4.2.197}}{{cite book |last1=Arnocky |first1=Steven |last2=Davis |first2=Adam |last3=Locke |first3=Ashley |last4=McKelvie |first4=Larissa |last5=Vaillancourt |first5=Tracy |chapter=Violence and Homicide Following Partner Infidelity |title=The Oxford Handbook of Infidelity |date=20 October 2022 |pages=516–554 |doi=10.1093/oxfordhb/9780197502891.013.26 |isbn=978-0-19-750289-1 |editor1=Tara DeLecce |editor2=Todd K. Shackelford }}
Other animals
As well as humans, EPC has been found in many other socially monogamous species.{{cite journal|last1=Houtman|first1=A. M.|title=Female Zebra Finches Choose Extra-Pair Copulations with Genetically Attractive Males|journal=Proceedings of the Royal Society B: Biological Sciences|date=1992-07-22|volume=249|issue=1324|pages=3–6|doi=10.1098/rspb.1992.0075|s2cid=83985353}} {{cite journal|last1=Gowaty|first1=P. A. |last2=Bridges |first2=W. C. |title=Behavioral, demographic, and environmental correlates of extrapair fertilizations in eastern bluebirds |journal=Behavioral Ecology |date=1991|volume=2|issue=4 |pages=339–350 |doi=10.1093/beheco/2.4.339}}{{cite journal |last1=Bollinger|first1=E. K.|last2=Gavin|first2=T. A.|title=Patterns of extra-pair fertilizations in bobolinks |journal= Behavioral Ecology and Sociobiology |date=1991| volume=29|issue=1|pages=1–7 |doi= 10.1007/BF00164288|bibcode=1991BEcoS..29....1B |s2cid=25208360}}{{r|ubl bundle}} 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).{{cite book |last1=Gowaty |first1=P. A. |editor1-last=Lucas |editor1-first=Jeffrey |editor2-last=Simmons |editor2-first=Leigh |title=Essays in animal behaviour: Celebrating 50 years of animal behaviour |date=2006 |publisher=Elsevier Academic Press |location=Burlington, MA |isbn=978-0-12-369499-7 |pages=221–254 |chapter=Beyond extra-pair paternity}}
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.{{cite journal|last1=Akçay|first1=E.|last2=Roughgarden|first2=J. |title= Extra-pair paternity in birds: Review of the genetic benefits|journal=Evolutionary Ecology Research |date=2007 |volume=9 |issue=5 |url-status=live |url=http://repository.upenn.edu/biology_papers/12 |access-date=2016-03-27 |archive-date=2016-04-19 |archive-url=https://web.archive.org/web/20160419032000/http://repository.upenn.edu/biology_papers/12/}}
=In birds=
File:Taeniopygia guttata -Bird Kingdom, Niagara Falls, Ontario, Canada -pair-8a.jpg: Bird Kingdom, Niagara Falls, Ontario, Canada]]
Extra-pair copulation is common in birds.{{cite book |last1=Welty |first1=J. C. |last2=Baptista |first2=L. F. |title=The life of birds |date=1988 |publisher=Saunders College Pub. |location=New York |isbn=978-0-03-068923-9 |edition=4th}} For example, zebra finches, although socially monogamous, are not sexually monogamous and hence do engage in extra-pair courtship and attempts at copulation.{{cite book |last1=Birkhead |first1=T. |last2=Parker |first2=G. |editor1-last=Krebs |editor1-first=John |editor2-last=Davies |editor2-first=Nicholas |title=Behavioural ecology: an evolutionary approach |date=1996 |publisher=Blackwell Science |location=Cambridge |isbn=978-0-86542-731-0 |pages=121–145 |edition=4th |chapter=Sperm competition and mating systems}} 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 versus many copulations with the other male.{{cite journal |last1=Birkhead |first1=T. R. |last2=Pellatt |first2=J. |last3=Hunter |first3=F. M. |title=Extra-pair copulation and sperm competition in the zebra finch |journal=Nature |date=1988 |volume=334 |issue=6177 |pages=60–62 |doi=10.1038/334060a0|pmid=3386741 |bibcode=1988Natur.334...60B |s2cid=4355745 }} EPC proportion varies between different species of birds.{{r|Petrie 1998}} For example, in eastern bluebirds, studies have shown that around 35% of offspring is due to EPC. Some of the highest levels of EPP are found in the New Zealand hihi or stitchbird (Notiomystis cincta), in which up to 79% of offspring are sired by EPC.{{cite journal |last1=Brekke |first1=Patricia |title=Evolution of extreme-mating behaviour: Patterns of extrapair paternity in a species with forced extrapair copulation |journal=Behavioral Ecology and Sociobiology |date=2013 |volume=67 |issue=6 |pages=963–972 |doi=10.1007/s00265-013-1522-9 |bibcode=2013BEcoS..67..963B |s2cid=17937763 |ref=Brekke 2013}} EPC can have significant consequences for parental care, as shown in azure-winged magpie (Cyanopica cyanus).{{Cite journal |date=2020 |last1= Gao |first1=Li-Fang|last2=Zhang|first2=Hai-Yang|last3=Zhang|first3=Wen|last4=Sun|first4=Yuan-Hai|last5=Liang|first5=Mao-Jun |last6=Du |first6=Bo |title=Effects of extra-pair paternity and maternity on the provisioning strategies of the Azure-winged Magpie Cyanopica cyanus |language=en|volume=162|issue=3|pages=627–636 |doi=10.1111/ibi.12800|s2cid=209585885 |url=https://onlinelibrary.wiley.com/doi/abs/10.1111/ibi.12800|journal=Ibis|issn=1474-919X|url-access=subscription}}
In socially polygynous birds, EPC 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.{{cite journal|last1=Hasselquist|first1=D.|last2=Sherman|first2=P.|title=Social mating systems and extrapair fertilizations in passerine birds|journal=Behavioral Ecology|date=2001|volume=12|issue=4|pages=457–466|doi=10.1093/beheco/12.4.457|doi-access=free}}
=In mammals=
File:Hylobates lar pair of white and black 02.jpg]]
EPC has been shown in monogamous mammals, such as the white-handed gibbon.{{cite journal |last1=Palombit |first1=Ryne A. |title=Extra-pair copulations in a monogamous ape |journal=Animal Behaviour |date=1994 |volume=47 |issue=3 |pages=721–723 |doi=10.1006/anbe.1994.1097 |s2cid=53197373 |url=http://rci.rutgers.edu/~palombit/Palombit_1994b.pdf |access-date=2018-07-21 |archive-url=https://web.archive.org/web/20180305000246/http://www.rci.rutgers.edu/~palombit/Palombit_1994b.pdf |archive-date=2018-03-05 |url-status=dead }} A study of one group found 88% in-pair copulation and 12% extra-pair copulation.{{cite journal |last1=Reichard |first1=U. |title=Extra-pair Copulations in a Monogamous Gibbon (Hylobates lar) |journal=Ethology |date=1995 |volume=100 |issue=2 |pages=99–112 |doi=10.1111/j.1439-0310.1995.tb00319.x|bibcode=1995Ethol.100...99R }} However, there is much variability in rates of EPC in mammals. One study found that this disparity in EPC is better predicted by the differing social structures of different mammals, rather than differing types of pair bonding. For example, EPC was lower in species who live in pairs compared to those who live in solitary or family structures.{{cite journal|last1=Cohas|first1=A.|last2=Allaine|first2=D.|title=Social structure influences extra-pair paternity in socially monogamous mammals|journal=Biology Letters|date=2009-03-04|volume=5|issue=3|pages=313–316|doi=10.1098/rsbl.2008.0760|pmid=19324647|pmc=2679913}}
=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.{{cite journal|last1=Gray|first1=E. M.|title=Do female red-winged blackbirds benefit genetically from seeking extra-pair copulations?|journal=Animal Behaviour|date=1997|volume=53|issue=3|pages=605–623|doi=10.1006/anbe.1996.0337|s2cid=53182918}} For example, in swallows, males with longer tails are involved in EPC more than those with shorter tails.{{cite journal|last1=Møller|first1=A.P.|title=Female choice selects for male sexual tail ornaments in the monogamous swallow|journal=Nature|date=1988-04-14|volume=332|issue=6165|pages=640–642|doi=10.1038/332640a0|bibcode=1988Natur.332..640M |s2cid=33212719}} 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.{{cite journal|last1=Smith|first1=S. M.|title=Extra-Pair Copulations in Black-Capped Chickadees: the Role of the Female|journal=Behaviour|date=January 1988|volume=107|issue=1|pages=15–23|doi=10.1163/156853988X00160}} 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.{{cite journal |last1=Forstmeier |date=2014 |first1=Wolfgang |last2=Nakagawa |first2=Shinichi|last3=Griffith|first3=Simon C.|last4=Kempenaers|first4=Bart|title=Female extra-pair mating: adaptation or genetic constraint?|journal=Trends in Ecology & Evolution|volume=29|issue=8 |pages=456–464|issn=0169-5347|doi=10.1016/j.tree.2014.05.005|pmid=24909948|bibcode=2014TEcoE..29..456F }}
Notes
{{notelist|refs=
{{efn|name="IPV"|text=Although sexual rivalry as a motive for intimate-partner violence (IPV) against males in heterosexual relationships is relatively rare,{{multiref2
|1={{cite journal |last1=Wilson |first1=Margo |last2=Daly |first2=Martin |title=An evolutionary psychological perspective on male sexual proprietariness and violence against wives |journal=Violence and Victims |date=1993 |volume=8 |issue=3 |pages=271–294 |doi=10.1891/0886-6708.8.3.271 |pmid=8186185|ref=none}}
|2={{cite journal |last1=Wilson |first1=Margo |last2=Daly |first2=Martin |title=Male sexual proprietariness and violence against wives |ref=none |journal=Current Directions in Psychological Science |volume=5 |number=1 |date=February 1996|pages=2–7|doi=10.1111/1467-8721.ep10772668 |url=http://faculty.knox.edu/fmcandre/male_sexual_proprietariness.pdf}} }} researchers have noted a small proportion of female partners assaulting or even killing males as being motivated by sexual jealousy, within the relatively smaller number of female-perpetrated (compared to male-perpetrated) IPV.{{r|koehler 2007|belknap}} Spousal homicide overall is more likely to be committed by males than females, as is having a sexual jealousy motivation for such homicides,{{cite book |last1=Daly |first1=Martin |last2=Wilson |first2=Margo |title=Homicide|date=1988|publisher=Aldine de Gruyter |location=Hawthorne, New York, US |isbn=978-0202011776 |chapter=Till Death Us Do Part |pages=187–213|url=https://archive.org/details/homicide0000daly/page/n7/mode/2up |url-access=subscription}}{{r|undoc|pp=18–19}} which suggests this risk from engaging in EPC is more pertinent for women than men. }}
}}
References
{{Reflist|refs=
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| For white-crowned sparrows, see,
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{{cite journal |last1= Kitchen |first1=A. M. |last2=Gese |first2=E. M. |last3=Waits |first3=L. P. |last4=Karki |first4=S. M. |last5=Schauster |first5=E. R. |ref= none |title=Multiple breeding strategies in the swift fox, Vulpes velox |journal=Animal Behaviour |date=2006 |volume=71 |issue=5 |pages=1029–1038 |s2cid=20780520 |doi=10.1016/j.anbehav.2005.06.015 |url=http://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1104&context=icwdm_usdanwrc |access-date=2019-09-18 |archive-date=2018-07-23 |archive-url= https://web.archive.org/web/20180723034801/https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1104&context=icwdm_usdanwrc |url-status=live|url-access=subscription }}
| For meerkats, see,
{{cite journal|last1=Young|first1=A. J.|last2=Spong|first2=G.|last3=Clutton-Brock|first3=T.|title=Subordinate male meerkats prospect for extra-group paternity: Alternative reproductive tactics in a cooperative mammal|journal=Proceedings of the Royal Society B: Biological Sciences |ref=none |date=2007-07-07 |volume=274 |issue=1618|pages=1603–1609|doi=10.1098/rspb.2007.0316|pmid=17456454|pmc=2169281}} }}
}}
Category:Developmental biology