A ticket to ride - Allele delivery by rail in secondary ruderal colonization by Arabidopsis arenosa

Human-generated ruderal habitats are abundant, but challenging for plants. Some ruderal habitats, however, provide networked corridors (e.g. roadsides and railways) that can facilitate rapid long-distance spread of successfully adapted variants. Here we use transcriptomic and genomic analyses, coupled with genetic mapping and transgenics to understand adaptation to railways in Arabidopsis arenosa. We show normally perennial A. arenosa switched to rapid cycling, a common adaptation for ruderal plants, at least twice upon railway colonization. We further show substantial gene flow from a widely distributed railway colonist likely contributed to secondary colonization by a non-ruderal type, highlighting how connectivity can affect adaptability. We find loss of expression of the reproductive repressor FLOWERING LOCUS C (FLC) is likely primarily responsible for rapid cycling in the widely distributed railway variant. However, a second railway colonist in the Alps also cycles rapidly, but retains high FLC. Some alleles in this population encode non-functional proteins, suggesting FLC has started to decay, but most are functional. Instead, this population likely circumvents FLC via a derived allele of CONSTANS (CO), which shows strong evidence of selection in this population. Importantly, we find this CO allele arrived via gene flow from the widespread ruderal, where it was also previously under selection. This suggests ruderal adaptation may have been progressive, perhaps in both cases, with FLC-circumvention arising first, and FLC loss arising later but ultimately obscuring its earlier circumvention. These snapshots of railway adaptation highlight that gene flow from widespread ruderals can provide opportunities for subsequent adaptation by local genotypes.