The evolutionary history of Cardamine bulbifera shows a successful rapid postglacial Eurasian range expansion in the absence of sexual reproduction

Background and Aims Sexual reproduction is known to drive plant
diversification and adaptation. Here we investigate the evolutionary
history and spatiotemporal origin of a dodecaploid (2n = 12x = 96)
Eurasian deciduous woodland species, Cardamine bulbifera, which reproduces
and spreads via vegetative bulb-like structures only. The species has been
among the most successful range-expanding understorey woodland plants in
Europe, which raises the question of the genetic architecture of its gene
pool, since its hexaploid (2n = 6x = 48) but putatively outcrossing
closest relative, C. quinquefolia, displays a smaller distribution range
in Eastern Europe towards the Caucasus region. Cardamine bulbifera belongs
to a small monophyletic clade of four species comprising also C. abchasica
(2n = 2x = 16) and C. bipinnata (unknown ploidy) from the Caucasus region.
Methods We sequenced the genomes of the two polyploids and their two
putative ancestors using Illumina short-read sequencing technology (×7–8
coverage). Covering the entire distribution range, genomic data were
generated for 67 samples of the two polyploids (51 samples of C.
bulbifera, 16 samples of C. quinquefolia) and 6 samples of the putative
diploid taxa (4 samples of C. abchasica, 2 samples of C. bipinnata) to
unravel the evolutionary origin of the polyploid taxa using phylogenetic
reconstructions of biparentally and maternally inherited genetic sequence
data. Ploidy levels of C. bulbifera and C. quinquefolia were analysed by
comparative chromosome painting. We used genetic assignment analysis
(STRUCTURE) and approximate Bayesian computation (ABC) modelling to test
whether C. bulbifera represents genetically differentiated lineages and
addressed the hypothesis of its hybrid origin. Comparative ecological
modelling was applied to unravel possible niche differentiation among the
two polyploid species. Key Results Cardamine bulbifera was shown to be a
non-hybridogenous, auto-dodecaploid taxon of early Pleistocene origin, but
with a history of past gene flow with its hexaploid sister species C.
quinquefolia, likely during the last glacial maximum in shared refuge
areas in Eastern Europe towards Western Turkey and the Crimean Peninsula
region. The diploid Caucasian endemic C. abchasica is considered an
ancestral species, which also provides evidence for the origin of the
species complex in the Caucasus region. Cardamine bulbifera successfully
expanded its distribution range postglacially towards Central and Western
Europe accompanied by a transition to exclusively vegetative propagation.
Conclusions A transition to vegetative propagation in C. bulbifera is
hypothesized as the major innovation to rapidly expand its distribution
range following postglacially progressing woodland vegetation throughout
Europe. Preceding and introgressive gene flow from its sister species C.
quinquefolia in the joint refuge area is documented. This transition and
ecological differentiation may have been triggered by preceding
introgressive gene flow from its sister species in the joint East European
refuge areas.