Exploring the development and diversification of the unique Aquilegia nectar spur

Abstract

Angiosperms are the most species-rich and morphologically diverse group in the plant kingdom, yet are also the most recently evolved. The flower itself, unique to the angiosperms, is where much of this diversity is on display – variation in organ number, shape, size, identity, fusion, color, and organization has yielded the seemingly endless floral forms found in nature. Determining the developmental programs underlying their morphological variation is key to elucidating the evolutionary processes that generated their stunning biodiversity. However, much work on floral development to date has been done in species such as Arabidopsis that have relatively simple flowers and do not represent the complexity and diversity of the angiosperms, nor the equally complex partnerships with animal pollinators that have been a major driving force in flowering plant evolution. Aquilegia (columbine, Ranunculaceae) is an ideal model system for investigating these evolutionary and developmental processes. Their five flower petals each produce an elaborate nectar spur, which varies dramatically in length, shape, and color depending on what animal pollinates a given Aquilegia species. This diversity is the result of a recent rapid radiation, during which the genus experienced multiple independent pollinator shifts. In this dissertation, I investigate the developmental and genetic underpinnings of a bee-to-hummingbird shift in Aquilegia, with a focus on the changes in spur morphology that occurred during this crucial pollinator transition. Across chapters, I apply multiple approaches toward the unifying objective of understanding the mechanisms that facilitated the rapid morphological diversification of the genus. In Chapter 1, originally published in Evolution, I use QTL mapping in F2 hybrids of bee-pollinated A. brevistyla and its hummingbird-pollinated sister species A. canadensis to uncover the genetic architecture of 17 floral traits spanning color, nectar composition, and organ morphology. I propose a genetic model for anthocyanin evolutionary dynamics in the cross, and discover that a single major-effect locus on chromosome 7 is responsible for spur curvature. In Chapter 2, I characterize the development and transcriptomics of A. brevistyla and A. canadensis spurs. My work revealed the surprisingly complex developmental basis of evolutionary transitions in spur shape and identified key molecular players and processes for further investigation. In Chapter 3, I synthesize these datasets to identify a candidate gene in the major QTL for spur curvature.