Abstract

The good genes hypothesis has long been a major focus of research on the function of extrapair (EP) behaviour by socially monogamous females. It predicts that females should be less faithful when paired to low-quality males and, as EP males become increasingly superior to their social mates, that EP males should be of higher quality than the males they cuckold. Evaluations have yielded mixed results, perhaps in part due to an overly strict interpretation of these predictions. A recent theoretical model demonstrated that while females with high-quality mates should be selective, those with low-quality males may gain good genes benefits by random EP mating, provided EP choosiness has costs, phenotypic indicators are imperfect and sperm competition favours genetic quality. We tested these classic and modified behavioural predictions in the blue-footed booby, Sula nebouxii , at two critical steps of EP interactions: courtship and copulation. Support for the classic good genes predictions was limited: EP courtship was more common in females with younger mates, but EP copulation following courtship was not predicted by social mate or relative male age, body size, condition, foot colour (a dynamic ornament) or breeding success, and these characteristics did not differ consistently between social and EP males. However, EP copulation increased with relative attractiveness (greener feet) of the EP male only when the social male was attractive, supporting the model's prediction that female choosiness should increase with social male attractiveness. Moreover, EP copulation probability decreased as EP males became increasingly superior to unattractive females, suggesting that EP males can also be choosy and may constrain female behaviour. Our results confirm that EP interactions involve more complexity than originally envisioned, warranting further studies that focus on behaviour and include all three main players: female, social mate and EP male. • We evaluated the good genes hypothesis of extrapair (EP) courtship and copulation in blue-footed boobies. • We also tested whether females with high-quality mates are choosier towards EP males. • Young males were more likely to be cuckolded, but social and EP male quality was similar. • Superior EP attractiveness increased EP copulation only in mates of attractive males. • Evidence for good genes was mixed, but results support flexible female EP choosiness.

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