Abstract
One key hypothesis explaining the evolution and persistence of polyandry, and resulting female extra‐pair reproduction in socially monogamous systems, is that female propensity for extra‐pair reproduction is positively genetically correlated with male reproductive fitness and consequently experiences positive cross‐sex indirect selection. However, key genetic correlations have rarely been estimated, especially in free‐living populations experiencing natural (co)variation in reproductive strategies and fitness. We used long‐term life‐history and pedigree data from song sparrows (Melospiza melodia) to estimate the cross‐sex genetic correlation between female propensity for extra‐pair reproduction and adult male lifetime reproductive success, and thereby test a key hypothesis regarding mating system evolution. There was substantial additive genetic variance in both traits, providing substantial potential for indirect selection on female reproductive strategy. However, the cross‐sex genetic correlation was estimated to be close to zero. Such small correlations might arise because male reproductive success achieved through extra‐pair paternity was strongly positively genetically correlated with success achieved through within‐pair paternity, implying that the same successful males commonly sire offspring produced by polyandrous and monogamous females. Cross‐sex indirect selection may consequently have limited capacity to drive evolution of female extra‐pair reproduction, or hence underlying polyandry, in systems where multiple routes to paternity success exist.
Highlights
Why do females commonly mate with multiple males when a single mating would seemingly suffice to fertilize a female’s eggs and ensure her reproductive success? Such female multiple mating, known as polyandry, is widely observed across the animal kingdom but is hard to explain because multiple mating is often harmful for females
We discovered that female extra-pair reproduction and male reproductive success both have a substantial genetic basis
Female extra-pair reproduction per brood (EPR) was observed for 1096 breeding attempts made by 279 individual females, and lifetime reproductive success (LRS) was observed for 306 adult males (Fig. 1A and B)
Summary
Why do females commonly mate with multiple males when a single mating would seemingly suffice to fertilize a female’s eggs and ensure her reproductive success? Such female multiple mating, known as polyandry, is widely observed across the animal kingdom but is hard to explain because multiple mating is often harmful for females. Males that mate extensively are likely to produce offspring with females that are willing to mate multiply (i.e., that are polyandrous). These offspring will inherit genes for multiple mating from their mother and genes for high reproductive success from their father, causing these sets of genes to become associated. The key idea that genes underlying female multiple mating are associated with genes underlying high male reproductive success has not yet been tested in wild populations where individuals are free to mate as they choose. Our study does not support the idea that female promiscuity is a side-product of selection on males
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