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

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 favour a preference for rarity. Indeed, we find that drift, by constantly perturbing male display allele frequencies, provides the fuel required to favour 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.

实验室与野外研究的证据表明，雌性有时会偏好拥有稀有表型（phenotype）的雄性。这一发现带来了理论层面的挑战：对稀有表型的偏好会降低该表型的稀有程度，进而降低携带该表型的雄性后代的适合度（fitness）。此外，对稀有性状的偏好会引发负频率依赖选择（negative frequency-dependent selection），使得雄性各类表型的占比趋于均等，从而消解了这类偏好的进化优势。如此一来，在众多分类群（taxa）中均观测到对稀有表型的偏好，便显得颇为矛盾。遗传漂变（genetic drift）通过推动等位基因（allele）的随机固定或丢失，持续成为稀有表型的产生动因。本研究旨在探讨有限种群规模是否能够为稀有表型偏好的演化提供必要的有利条件。研究结果表明，遗传漂变通过持续扰动雄性展示性状相关等位基因的频率，为青睐稀有表型的雌性偏好等位基因的传播提供了必要动力。当该偏好等位基因扩散后，雄性展示性状基因座（locus）上产生的负频率依赖选择，便可维持雄性展示饰物的表型多样性。由此可见，遗传漂变通过助力维持表型多样性，发挥了非典型的演化作用。此外，本研究还发现，在多斑块生境中，这一效应会更为显著。本研究为雌性稀有表型偏好的多次独立演化提供了一种全新的潜在解释。