Extra pair paternity occurs when the female of a partner of a pair bonded couple engages in extra pair copulations (i.e. copulation with a male other than the bonded male) and as a result gives birth to offspring whose father is not the bonded male. The level of extra-pair paternity varies greatly, being absent in some species, whilst in other species it is an absolute necessity to the breeding strategy. Variation can even occur within the same genus or even species.
In many avian mating systems, the female is able to control the success of copulation and the transfer of sperm from the male to the female. Because of this, extra-pair copulations will only result in extra-pair paternity should the female choose. The female would only choose such a situation if it were beneficial for her to modify the paternity (and thus genetics) of her clutch. In an attempt to reduce the impact on fitness of the bonded male, in some species, the males have evolved counter strategies to prevent the loss of paternity. These include frequent copulation and even forced copulation should the male suspect that the female has engaged in extra-pair copulation.
Females engage in extra-pair copulations in an attempt to gain ‘good genes’ which would benefit the genetic fitness of her offspring. A female pair bonded to a male of poor genetic quality is much more likely to engage in extra-pair copulations with males of a greater genetic quality, thus improving the survivability and reproductive success of her offspring (ultimately continuing the spread of her genes). In populations where the genetic quality of males is highly variable, there are many more extra-pair copulations as the difference between a genetically poor and high quality male can be quite large.
The degree to which a population varies in genetic fitness can be geographical and depend on certain factors such as the prevalence of diseases and parasites. Isolated geographical regions, such as islands, typically have low genetic diversity amongst the species. As a result, the number of extra pair copulations is generally quite low.
Females may also seek to engage in extra-pair copulations to reduce the cost of mate loss. For instance, if a fertile female is not fertilised by the pair-bonded male she is essentially wasting her time as she will not be raising offspring. To ensure that this is not the case, females will actively seek extra-pair copulations to ensure she is fertilised and thus has a brood to raise.
Whilst extra-pair copulations are arguably primarily conducted to gain genetic benefits, some females also engage in them to receive direct benefits. Benefits such as:
The opportunity to forage in the territory of the new male
Additional protection, especially if the extra-copulatory male was a close neighbour
The act of extra-pair copulations for direct benefit therefore depends on the resource availability (i.e. if resource availability is high, then the female has no need to engage in extra-pair copulation for direct benefit) and the distance to the nearest neighbour (a distant neighbour will not offer much protection).
It may be that frequent copulation with the same male causes his sperm levels to deplete. In such a case, it is again beneficial for the female to engage in extra-pair copulations with other males. She needs to ensure that her eggs are not laid unfertilised.
Ultimately, whether or not a female engages in extra-pair copulations, depends on their cost. If the cost is low and therefore the female has more to gain from an extra-pair copulation she is highly likely to engage in such. The major cost to the female is that the pair bonded male loses interest in her and the investment time he would spend in raising her offspring following extra-pair copulation. In avian species where bi-parental care is of great importance to chick survival it is therefore much less likely extra-pair copulations will occur as the female has too much to lose i.e. it is much more likely her offspring will die. However, if male parental investment has little influence of offspring survival, it is beneficial for the female to engage in extra-pair copulations. Other costs of extra-pair copulations include; the physical energy put into finding another male (varies depending on the density of the colony) and the probability that the female will obtain sexually transmitted disease from the other males.
The behaviour of the pair is also an important factor, for instance bonded males can act aggressively towards other males and guard the female, which obviously reduces the chance she will engage in extra-pair copulations. The same is true of females, if a female allows her male to engage in extra-pair copulations she is risking disease, loss of male investment and the depletion of her partner’s sperm. It is therefore also beneficial for the females to act aggressively towards other females and engage in mate guarding.
Social and Sexual Monogamy (Morell 1998)
Social monogamy and sexual monogamy are in fact quite different. True sexual monogamy is when the male and female remain with one another and do not mate with anyone outside the pair. Social monogamy on the other hand occurs when the male and female remain in a partnership but copulation does occur with other males and females outside of the pair bond. Social monogamy is commonplace in birds, but true sexual fidelity is much less common. Because of this, it is often the case that some of the female’s offspring are actually not the offspring of the partnered male (extra-pair paternity).
It was once thought that males within a pair bond would only raise offspring that were his own, but it is now known this is not the case. Bi-parental care is often an important part of offspring survival due to the labour intensive requirements of incubation and feeding, however only around 10% of avian species are truly monogamous.
Females must have a good reason to engage in extra-pair copulations, the reason usually being to improve the genetics of her offspring. The female must actively receive sperm (it is believed in some species the female can ‘dump’ the sperm) and thus it is the female who can essentially control extra-pair paternity. The female may want to alter the genetics of her offspring between clutches to ensure she has multiple offspring with a wide variety of genetics; this increases the chance that her offspring will adapt and survive should there be a sudden environmental change.
In some cases, the female’s choice of initial partner will depend on his access to resources. Seeing as this initial partner is the male with which the female will pair bond (social monogamy) it is beneficial for the female (and thus her offspring) if he has a high quality nest, with access to good foraging grounds. It doesn’t matter if the male is of poor genetic quality because the female can actively engage in extra-pair copulations with males of a higher genetic standard.
Female Great Reed Warblers prefer males with a large song repertoire as this often indicates better genetic quality. Because of this, females pair bonded to males of poor genetic quality are much more likely to seek out males of higher genetic quality. The increase in fitness of the extra-copulatory male will benefit her offspring. The male will stay with the female as it is the best way to ensure the survival of his offspring. In some species, such as bluebirds, the density of nests also puts him in a good position to mate with other neighbouring females.
Whether or not true sexual fidelity occurs depends on how essential bi-parental care is to the survival of the offspring. Whilst the need can vary greatly in birds (e.g. from 0% chick survivability in large raptor species to 50+% in smaller species) in some species such as the California mouse it is essential. The Californian mouse is completely monogamous because bi-parental care is essential for the survival of their offspring. If either parent leaves, the offspring will die – this is due to the environment which they inhabit being relatively cold; one parent must stay with the offspring constantly to ensure warmth, whilst the other forages for food. Interestingly, a similar species of rodent, which inhabits the same environment, engages in a promiscuous mating system.
It is possible that there is a link between hormones and sexual monogamy. In Prairie voles, it has been observed that during a 24 hour period, a single male and female will engage in multiple copulations. These copulations result in a large release of neuropeptides which is believed to be responsible for the resulting formation of strong pair bonds. However, this neuropeptides is also produced in all other males (even promiscuous species). The difference is the location of the neuropeptides receptor, it is thought that because the receptors are located in completely different places, they are able to have different roles – hence why the hormone can form strong pair bonds in one species, but not another.
In summary, tending a nest or offspring is always going to be easier with two committed parents. Mothers evolved requiring help to raise offspring and as a result the evolution of social monogamy was favoured.
Morell, V. 1998, “A new look at monogamy”, Science, vol. 281, no. 5385, pp. 1982-1983.
Petrie, M. & Kempenaers, B. 1998, “Extra-pair paternity in birds: Explaining variation between species and populations”, Trends in Ecology and Evolution, vol. 13, no. 2, pp. 52-57.