Evolution of the Sabulina verna group (Caryophyllaceae) in Europe: A deep split, followed by secondary contacts, multiple allopolyploidization and colonization of challenging substrates

One of the major goals of contemporary evolutionary biology is to
elucidate the relative roles of allopatric and ecological differentiation
and polyploidy in speciation. In this study, we address the taxonomically
intricate Sabulina verna group, which has a disjunct Arctic–alpine
postglacial range in Europe and occupies a broad range of ecological
niches, including substrates toxic to plants. Using genome-wide ddRAD
sequencing combined with morphometric analyses based on extensive sampling
of 111 natural populations, we aimed to disentangle internal evolutionary
relationships and examine their correspondence with the pronounced edaphic
and ploidy diversity within the group. We identified two spatially
distinct groups of diploids: a widespread Arctic–alpine group and a
spatially restricted yet diverse Balkan group. Most tetraploids exhibited
a considerably admixed ancestry derived from both these groups, suggesting
their allopolyploid origin. Four genetic clusters in congruence with
geography and mostly supported by morphological traits were recognized in
the diploid Arctic–alpine group. Tetraploids are split into two distinct
and geographically vicariant groups, indicating their repeated polytopic
origin. Furthermore, our results also revealed at least five-fold parallel
colonization of toxic substrates (serpentine and metalliferous),
altogether demonstrating a complex interaction between geography,
challenging substrates, and polyploidy in the evolution of the group.
Finally, we propose a new taxonomic treatment of this intricate complex.