Extra-pair paternity (EPP) challenges traditional assumptions about mating systems in the animal kingdom. Advances in molecular biology have revealed a disconnect between social relationships and genetic parentage, particularly in species like birds that were once assumed to be strictly faithful. EPP shows that reproductive strategies often prioritize maximizing individual fitness over pair-bond fidelity. Its prevalence across diverse taxa demonstrates that evolutionary pressures favor flexibility in mating behaviors, even among socially monogamous species.
Defining Extra Pair Paternity
Extra-pair paternity occurs when a female mates with a male other than her social partner, and that male successfully sires offspring that are subsequently raised within the pair-bonded unit. This outcome forces a distinction between two types of mating systems: social monogamy and genetic monogamy. Social monogamy describes a pair bond where a male and female cooperate to raise offspring, often sharing parental duties like nest defense and foraging for food.
Genetic monogamy, by contrast, is a much rarer situation where all offspring produced by the pair are exclusively sired by the social male. In many species, especially birds, the use of DNA analysis has shown that social monogamy frequently coexists with EPP, sometimes at very high rates. The resulting offspring are referred to as extra-pair young (EPY) and are genetically unrelated to the social father, despite him providing parental care.
Behavioral Mechanisms and Species Occurrence
The genetic outcome of EPP is the result of a specific behavior known as extra-pair copulation (EPC), which is a mating event between a member of a pair bond and an individual outside that bond. These copulations can be actively sought by either the male or the female, or they can occur as a result of forced matings by an extra-pair male. The frequency and context of these matings are highly variable, often depending on local ecological factors like breeding density and the availability of potential extra-pair mates.
EPP is most extensively studied in Aves, or birds, where over 75% of socially monogamous species exhibit some level of it. For instance, certain bluebird populations can have up to 35% of offspring sired by extra-pair males, and some passerine species show rates as high as 76%. This reproductive strategy is also documented in various socially bonded mammals, including certain primates and rodents.
Evolutionary Drivers for Individual Fitness
The persistence of EPP is rooted in the fitness benefits it offers to both sexes, despite the social costs involved.
Female Drivers
For females, the primary drivers are often indirect genetic benefits, such as the “good genes” hypothesis. A female paired to a lower-quality social mate may seek an EPC with a genetically superior male. This strategy allows her to gain high-quality genes for her young while retaining the parental investment and territory defense provided by her social partner.
Another benefit for females is the “compatible genes” hypothesis, which suggests females seek extra-pair partners whose genes are better suited to combine with their own, potentially increasing offspring viability. Mating with a genetically dissimilar male can also increase the overall genetic diversity of a clutch, which may buffer against environmental changes or disease.
Male Drivers
For males, the advantage of engaging in EPCs is straightforward: it is a low-cost way to maximize reproductive success. Males can sire offspring in multiple nests without dedicating time or energy to their parental care. Successfully engaging in EPCs increases the total number of genes they pass on, which is a direct measure of evolutionary fitness.
Consequences for Population Genetics and Social Structure
EPP has significant consequences that extend beyond the immediate family unit to affect the entire population. From a genetic perspective, EPP acts as a mechanism for increasing the overall genetic variation within a population by facilitating gene flow between social groups. This increased diversity is beneficial because it can reduce the likelihood of inbreeding, especially in small or isolated populations.
EPP also shapes the social structure and behavior of a species, particularly concerning parental investment and male-male competition. Since males risk investing in offspring that are not theirs, a negative correlation can evolve where higher rates of EPP lead to a reduction in paternal care by the social male. In response, males may evolve mate-guarding behaviors to prevent their social female from seeking extra-pair copulations, or they may shift their investment to communal benefits within the neighborhood, as they are likely to have extra-pair offspring nearby. The increased variance in male reproductive success driven by EPP also intensifies sexual selection, leading to the evolution of pronounced secondary sexual characteristics, such as brighter plumage or larger body size in successful extra-pair sires.