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Understanding the evolutionary factors that impact the genetic architecture of traits is a central goal of evolutionary genetics. Here, we investigate how quantitative trait variation accumulated over time in populations that colonized a novel environment. We compare the genetic architecture of flowering time in Arabidopsis populations from the drought-prone Cape Verde Islands and their closest outgroup population from North Africa. We find that trait polygenicity is severely reduced in the island populations compared to the continental North African population. Further, trait architectures and reconstructed allelic histories best fit a model of strong directional selection in the islands in accord with a Fisher–Orr adaptive walk. Consistent with this, we find that large-effect variants that disrupt major flowering time genes (FRI and FLC) arose first, followed by smaller effect variants, including ATX2 L125F, which is associated with a 4-day reduction in flowering time. The most recently arising flowering timeassociated loci are not known to be directly involved in flowering time, consistent with an omnigenic signature developing as the population approaches its trait optimum. Surprisingly, we find no effect in the natural population of EDI-Cvi-0 (CRY2 V367M), an allele for which an effect was previously validated by introgression into a Eurasian line. Instead, our results suggest the previously observed effect of the EDI-Cvi-0 allele on flowering time likely depends on genetic background, due to an epistatic interaction. Altogether, our results provide an empirical example of the effects demographic history and selection has on trait architecture., Understanding the evolutionary factors that impact the genetic architecture of traits is a central goal of evolutionary genetics. Here, we investigate how quantitative trait variation accumulated over time in populations that colonized a novel environment. We compare the genetic architecture of flowering time in Arabidopsis populations from the drought-prone Cape Verde Islands and their closest outgroup population from North Africa. We find that trait polygenicity is severely reduced in the island populations compared to the continental North African population. Further, trait architectures and reconstructed allelic histories best fit a model of strong directional selection in the islands in accord with a Fisher-Orr adaptive walk. Consistent with this, we find that large-effect variants that disrupt major flowering time genes (FRI and FLC) arose first, followed by smaller effect variants, including ATX2 L125F, which is associated with a 4-day reduction in flowering time. The most recently arising flowering time-associated loci are not known to be directly involved in flowering time, consistent with an omnigenic signature developing as the population approaches its trait optimum. Surprisingly, we find no effect in the natural population of EDI-Cvi-0 (CRY2 V367M), an allele for which an effect was previously validated by introgression into a Eurasian line. Instead, our results suggest the previously observed effect of the EDI-Cvi-0 allele on flowering time likely depends on genetic background, due to an epistatic interaction. Altogether, our results provide an empirical example of the effects demographic history and selection has on trait architecture.

Understanding how organisms adapt to new environments is a key goal of evolutionary biology. Populations subject to abrupt environmental change must adapt quickly to avoid extinction. Small populations are especially vulnerable to habitat changes, confronting high extinction risk due to limited genetic variation and low efficiency of selection. Theory predicts that the age of a population and its long- term effective size should influence adaptation and trait architecture. Here, we investigate the mechanisms of adaptation after a sudden shift to a more arid climate using natural populations of Arabidopsis thaliana in Cape Verde (CVI). CVI Arabidopsis is found on two islands (Santo Antão and Fogo) and represents diverged, monophyletic lineages based on the near absence of shared polymorphisms with each other or the continent. Time to flowering was reduced in parallel on the islands, causing a consequent increase in fitness, and allowing adaptation to the arid CVI. This change was mediated by convergent de novo loss of function of two core flowering time genes: FRI in Santo Antão and FLC in Fogo. Our results reveal a case where expansion of the new populations coincided with the emergence and proliferation of these novel variants, consistent with models of rapid adaptation and evolutionary rescue. We further contrast the genetic architecture of flowering time in the recently formed small Ne Arabidopsis lineages from Cape Verde with their much older, larger Ne progenitor – the Moroccan population. We find that polygenicity is severely reduced in the colonizing populations and effect sizes of candidate loci are exponentially distributed, consistent with fitness measures showing evidence for directional selection in the islands. In addition to the major effect variants FRI K232X and FLC R3X, we identify candidate variants from core flowering time pathways as well as those that indirectly affect flowering time, including nutrient processing and light sensing. Surprisingly

Most well-characterized cases of adaptation involve single genetic loci. Theory suggests that multilocus adaptive walks should be common, but these are challenging to identify in natural populations. Here, we combine trait mapping with population genetic modeling to show that a two-step process rewired nutrient homeostasis in a population of Arabidopsis as it colonized the base of an active stratovolcano characterized by extremely low soil manganese (Mn). First, a variant that disrupted the primary iron (Fe) uptake transporter gene (IRT1) swept quickly to fixation in a hard selective sweep, increasing Mn but limiting Fe in the leaves. Second, multiple independent tandem duplications occurred at NRAMP1 and together rose to near fixation in the island population, compensating the loss of IRT1 by improving Fe homeostasis. This study provides a clear case of a multilocus adaptive walk and reveals how genetic variants reshaped a phenotype and spread over space and time.