Genetic Architecture of Flowering Time Differs Between Populations With Contrasting Demographic and Selective Histories

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.