UC Santa Barbara

Broadly, the field of evolutionary biology aims to understand the spectrum of evolutionary mechanisms that generate the diversity of life. At one end of the spectrum is Darwinian gradualism – slow, gradual change driven by small effect mutations that likely accounts for an overwhelming majority of evolution over the past 4 billion years. At the other end sits saltational evolution – a mechanism that invokes large effect macromutations and evolutionary “leaps”. The most extreme version of saltational evolution is Richard Goldschmidt’s “hopeful monster”: a single, large effect macromutation (likely affecting early development) that drastically alters the body plan (e.g. homeotic mutants). This radical change would almost always be deleterious (“hopeless monster”), but on the rare occasion that this change occurred in the right ecological context, an entirely new lineage could arise. Unfortunately, natural evidence for hopeful monsters is almost nonexistent. For the first chapter of my dissertation, I begin by reviewing the current literature and report on a handful of studies that have identified large effect mutations that underly adaptive traits in nature and discuss why these examples do (or do not) fit into Goldschmidt’s criteria for a hopeful monster. I then review some oft-cited examples of hopeful monsters and how they fit into Goldschmidt’s criteria. Lastly, I introduce a case study for hopeful monsters. This is expanded upon in Chapter 2.

For my second chapter, I present my research on a naturally occurring homeotic mutant of the columbine Aquilegia coerulea, A. coerulea var. daileyae, in which the nectar-spurred petal is replaced with a second set of sepals, which do not produce nectar. Despite the expected negative effects of losing a pollinator reward, I find that floral herbivores, not pollinators, are driving strong, positive selection (s = 0.17-0.3) for the mutant morphology. Then, using population sequencing, haplotype analysis and SNP genotyping, I was able to identify the underlying locus (APETALA3-3) and multiple independently-derived causal loss-of-function mutations indicating an on-going soft-sweep. Elevated linkage disequilibrium around the two most common causal alleles indicates that positive selection has been ongoing for many generations. Furthermore, genotypic frequencies at AqAP3-3 indicate a degree of positive assortative mating by morphology, indicating that this morphological shift could lead to a new lineage. Lastly, I frame this homeotic shift in a macroevolutionary lens, showing not only that petal loss is a viable and stable macroevolutionary transition, but also that the genetic mechanism in this study population (loss of function at AP3-3) mimics the genetic mechanism at the macroevolutionary level. By identifying a large effect macromutation affecting early development that is under selection in the proper ecological setting and plays a role in mating patterns, I present some of the strongest evidence to date of a hopeful monster.