Non-pollinator selection for a floral homeotic mutant conferring loss of nectar reward in Aquilegia coerulea

Here, we describe a polymorphic population of Aquilegia coerulea with a naturally occurring floral homeotic mutant, A. coerulea var. daileyae, where the characteristic petals with nectar spurs are replaced with a second set of sepals. Although it would be expected that this loss of pollinator reward would be disadvantageous to the mutant, we find that it has reached relatively high frequency (∼25%) and is under strong, positive selection across multiple seasons (s = 0.17–0.3) primarily due to reduced floral herbivory. We identify the underlying locus (APETALA3-3) and multiple causal loss-of-function mutations indicating an ongoing soft sweep. Elevated linkage disequilibrium around the two most common causal alleles indicates that positive selection has been occurring for many generations. Lastly, genotypic frequencies at AqAP3-3 indicate a degree of positive assortative mating by morphology. Together, these data provide both a compelling example that large-scale discontinuous morphological changes differentiating taxa can occur due to single mutations and a particularly clear example of linking genotype, phenotype, and fitness. [Display omitted] •A petal-to-sepal homeotic mutant is abundant in an Aquilegia population•Reduced herbivory and resource allocation cause selection for the homeotic mutant•Multiple loss-of-function alleles in APETALA3-3 (AP3-3) cause the homeotic mutant•Genetic signatures at AP3-3 indicate a soft sweep and positive assortative mating Cabin et al. present a case of natural selection in action. They show that a floral homeotic mutant of Aquilegia is under strong positive selection primarily due to reduced floral herbivory. Loss-of-function alleles at APETALA3-3 underlie the phenotype and molecular signatures at the locus indicate a soft sweep and assortative mating by morphology.