Female guppies can recognize kin but only avoid incest when previously mated

Kin recognition plays a key role in inbreeding avoidance for taxa from all major animal groups; however, perplexingly, a number of species, for which the risks and costs of inbreeding are high, do not discriminate against relatives in mate choice experiments. We tested a possible explanation for this paradox: most tests of inbreeding avoidance have used virgin females, but theory predicts that virgin females should first mate indiscriminately to gain reproductive assurance and, only subsequently, become choosy. To test this idea, we used the Trinidadian guppy, which suffers inbreeding depression but for which evidence for kin recognition is equivocal. We manipulated rearing environment to disentangle 2 forms of kin recognition and tested the preferences of both virgin and nonvirgin females. As predicted, virgins were indiscriminate in their mate choice. Nonvirgins, in contrast, expressed strong preferences for unfamiliar and unrelated males. Therefore, female guppies recognize kin in a mate choice context but become selective only once reproductively assured. This dynamic likely increases population fitness in newly colonized or small, at-risk populations by ensuring that virgins mate even when only unfamiliar or unrelated males are available. Our findings suggest that inbreeding avoidance may be more common than previously thought and that the use of virgin females can sometimes prevent the detection of powerful mate preferences.