It is better to be choosy in small populations: drift promotes the evolution of weak female preference for rare...

Evidence from lab and field studies suggests that females sometimes prefer males bearing rare phenotypes. Such a finding poses a theoretical challenge, because preference for a rare phenotype makes that phenotype less rare, thereby lowering the fitness of sons bearing it. Further, a preference for rarity creates negative frequency-dependent selection, which leads to equal representation of male types. This then eliminates any benefit to a preference for rarity. It seems paradoxical, then, that preference for rarity has been observed across so many taxa. Genetic drift, by promoting stochastic fixation or loss of alleles, is a source of constant rarity. Here, we ask whether finite population sizes might provide the necessary conditions that favor a preference for rarity. Indeed, we find that drift, by constantly perturbing male display allele frequencies, provides the fuel required to favor a choosy female preference allele. Once this preference allele spreads, resultant negative frequency-dependent selection at the male display locus can act to maintain diversity in male display ornaments. Thus, drift plays an atypical role by helping maintain diversity. Further, we show that this finding is stronger in multi-patch landscapes. This work provides a novel potential explanation for the repeated evolution of female preference for rarity.