Pan-European study of genotypes and phenotypes in the Arabidopsis relative Cardamine hirsuta reveals how adaptation, demography, and development shape diversity patterns

by Lukas Baumgarten, Bjorn Pieper, Baoxing Song, Sébastien Mane, Janne Lempe, Jonathan Lamb, Elizabeth L. Cooke, Rachita Srivastava, Stefan Strütt, Danijela Žanko, Pedro GP Casimiro, Asis Hallab, Maria Cartolano, Alexander D. Tattersall, Bruno Huettel, Dmitry A. Filatov, Pavlos Pavlidis, Barbara Neuffer, Christos Bazakos, Hanno Schaefer, Richard Mott, Xiangchao Gan, Carlos Alonso-Blanco, Stefan Laurent, Miltos Tsiantis

We study natural DNA polymorphisms and associated phenotypes in the Arabidopsis relative Cardamine hirsuta. We observed strong genetic differentiation among several ancestry groups and broader distribution of Iberian relict strains in European C. hirsuta compared to Arabidopsis. We found synchronization between vegetative and reproductive development and a pervasive role for heterochronic pathways in shaping C. hirsuta natural variation. A single, fast-cycling ChFRIGIDA allele evolved adaptively allowing range expansion from glacial refugia, unlike Arabidopsis where multiple FRIGIDA haplotypes were involved. The Azores islands, where Arabidopsis is scarce, are a hotspot for C. hirsuta diversity. We identified a quantitative trait locus (QTL) in the heterochronic SPL9 transcription factor as a determinant of an Azorean morphotype. This QTL shows evidence for positive selection, and its distribution mirrors a climate gradient that broadly shaped the Azorean flora. Overall, we establish a framework to explore how the interplay of adaptation, demography, and development shaped diversity patterns of 2 related plant species.