Bet-hedging against male-caused reproductive failures may explain ubiquitous cuckoldry in female birds.

The origin and maintenance of polyandry is one of the key unresolved questions in evolutionary biology. In particular, extra-pair paternity (EPP) due to polyandry is observed in most (socially-) monogamous female birds and the frequency of EPP is surprisingly high (up to 72% in a clutch on average in some species). Many case-by-case hypotheses have been presented to explain this phenomenon but a ubiquitous explanation is still lacking. One possible general explanation is bet-hedging, which is a strategy to avoid the risk associated to mating with a single unsuitable male and thus to minimize the chances of complete reproductive failure by the female. Here, we present a mathematical solution to demonstrate that bet-hedging polyandry becomes highly effective if the risk of extinction of a female lineage attributable to male deficiencies is high in small subpopulation or under limited mate availability. Therefore, cuckoldry or polyandry may be a female strategy to spread the risk of extinction of her genotype over multiple males. The results agree well with the observed EPP frequencies in natural populations and the results of a meta-population simulation model. Our theory contributes new insights applicable not only to birds but also to a broad taxonomic range of animals.