The evolutionary history ofCardamine bulbiferashows a successful rapid postglacial Eurasian range expansion in the absence of sexual reproduction

Abstract

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 understory woodland plants in Europe, which raises the question of the genetic architecture of respective gene pools, 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 (7-8x 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 six 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 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. C. 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.

Evolutionary dynamics of Euphorbia carniolica suggest a complex Plio–Pleistocene history of understorey species of deciduous forest in southeastern Europe

“…At the same time, climatically induced vegetation fragmentation might have caused large‐scale extinctions of forest species in previously forested areas as indicated by the large distance between extant ranges of E. carniolica and its sister E. altaica ; a pattern that has been observed also in other DFUS of pre‐Pleistocene origin (Bartha et al, 2015 ; Sun et al, 2005 ; Yesson et al, 2009 ). Our findings complement evidence of pre‐Pleistocene origins of the DFUS Cyclamen purpurascens (Yesson et al, 2009 ), Cardamine enneaphyllos (L.) Crantz, C. trifolia L., C. waldsteinii Dyer (Huang et al, 2020 ; Ru et al, 2022 ), Euphorbia dulcis L. (this study; Figure S6 ) and Knautia drymeia (Rešetnik et al, 2016 ). However, the question if this pattern is pervasive for other (illyricoid) DFUS in southeastern Europe would need to be tested in a multispecies framework.…”