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

Zachary Cabin,Alexandra Garton,Ashley Quezada,Timothy Ngo,Scott A Hodges,Constantine Gasseholm,Nathan J Derieg,Mark Simon

doi:10.1016/j.cub.2022.01.066

Zachary Cabin, Alexandra Garton + Show 6 more

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https://doi.org/10.1016/j.cub.2022.01.066

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Journal: Current Biology	Publication Date: Feb 16, 2022
Citations: 9	License type: cc-by

Affiliation: University of California, Santa Barbara

Abstract

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.

Highlights

Floral herbivory favors homeotic mutant Across all three seasons we found significantly greater floral herbivory on We identified functional haplotypes (WT) flowers (Figure 3A)
We identified functional haplotypes (WT) as those that when heterozygous with a haplotype carrying a d mutation produce WT morphology
We found a significant preference by deer for WT plants in only one year, it has previously been shown that large mammal herbivory can be inconsistent across generations and still elicit a strong evolutionary response, even cancelling out and reversing selection driven by pollinators.[33,34]

Summary

Introduction

Darwin famously argued that evolution proceeds gradually through many changes of small effect, slowly improving one form over another.[1] Theory supported this view,[2] but later it was recognized that intermediate-effect size mutations are likely to contribute to adaptation.[3]. Comparative analyses show that changes in the number or expression patterns of genes involved in organ development (e.g., homeotic patterning genes[8–12] or organ symmetry genes13,14) are correlated with major morphological differences between taxa. Whether these differences evolved through single macromutations or the accumulation of many smaller changes is unknown. We have very little evidence that single homeotic mutations can and do survive in nature

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