So Closely Related and Yet So Different: Strong Contrasts Between the Evolutionary Histories of Species of the Cardamine pratensis Polyploid Complex in Central Europe

Abstract

Recurrent polyploid formation and weak reproductive barriers between independent polyploid lineages generate intricate species complexes with high diversity and reticulate evolutionary history. Uncovering the evolutionary processes that formed their present-day cytotypic and genetic structure is a challenging task. We studied the species complex of Cardamine pratensis, composed of diploid endemics in the European Mediterranean and diploid-polyploid lineages more widely distributed across Europe, focusing on the poorly understood variation in Central Europe. To elucidate the evolution of Central European populations we analyzed ploidy level and genome size variation, genetic patterns inferred from microsatellite markers and target enrichment of low-copy nuclear genes (Hyb-Seq), and environmental niche differentiation. We observed almost continuous variation in chromosome numbers and genome size in C. pratensis s.str., which is caused by the co-occurrence of euploid and dysploid cytotypes, along with aneuploids, and is likely accompanied by inter-cytotype mating. We inferred that the polyploid cytotypes of C. pratensis s.str. are both of single and multiple, spatially and temporally recurrent origins. The tetraploid Cardamine majovskyi evolved at least twice in different regions by autopolyploidy from diploid Cardamine matthioli. The extensive genome size and genetic variation of Cardamine rivularis reflects differentiation induced by the geographic isolation of disjunct populations, establishment of triploids of different origins, and hybridization with sympatric C. matthioli. Geographically structured genetic lineages identified in the species under study, which are also ecologically divergent, are interpreted as descendants from different source populations in multiple glacial refugia. The postglacial range expansion was accompanied by substantial genetic admixture between the lineages of C. pratensis s.str., which is reflected by diffuse borders in their contact zones. In conclusion, we identified an interplay of diverse processes that have driven the evolution of the species studied, including allopatric and ecological divergence, hybridization, multiple polyploid origins, and genetic reshuffling caused by Pleistocene climate-induced range dynamics.

Allele Sorting as a Novel Approach to Resolving the Origin of Allotetraploids Using Hyb-Seq Data: A Case Study of the Balkan Mountain Endemic Cardamine barbaraeoides

“…The relationships between the other four species, C. apennina , C. matthioli , C. penzesii , and C. rivularis , all traditionally classified within the C. pratensis group, showed conflicting patterns between nuclear and plastid trees but also low support ( Figure 7 ). Both ongoing and past gene flows, the latter probably facilitated by range shifts in glacial-interglacial periods, have been inferred to occur between C. matthioli and C. rivularis in Bulgaria ( Ančev et al, 2013 ; Melichárková et al, 2020 ), which may explain their close position in the plastid tree, in contrast to the nuclear tree. The lowland species C. penzesii was resolved as sister to C. uliginosa from the Caucasus in nuclear trees, whereas the positions of both species remained uncertain in plastome trees.…”

“…The studied species complexes comprise numerous endemics not only in the Balkan Peninsula but also across the other parts of the Mediterranean ( Marhold et al, 2018 ). The prevalence of endemics in the Mediterranean, along with the commonly observed geographically structured genetic variation within several species ( Lihová et al, 2003 ; Perný et al, 2005a , b ; Melichárková et al, 2020 ), suggests that geographic isolation played an important evolutionary role. These patterns may reflect past range fragmentation in response to Pleistocene climatic oscillations ( Nieto Feliner, 2014 ), as well as spatially restricted gene flow and species dispersal, which may be the two principal causes, acting in concert, of the current high endemism rate in these species complexes.…”

“…opicii (J. Presl et C. Presl) Čelak; Figure 1 ]. Apart from tetraploid records for C. barbaraeoides ( Perný et al, 2005a ; Lihová and Marhold, 2006 ], the other Balkan taxa are known to be diploid, with exceptional triploid plants reported for C. rivularis and C. × rhodopaea Ančev ( C. rivularis × C. matthioli ) ( Kučera et al, 2005 ; Ančev et al, 2013 ; Melichárková et al, 2020 ). Only diploid representatives have so far been reported from the adjacent Anatolian–Caucasus region ( Marhold et al, 2004 ; Kučera et al, 2005 ).…”

“…The design of the Cardamine -specific target enrichment probes is described in detail in Melichárková et al (2020) . In brief, we used genome skim data of Cardamine parviflora (NCBI accession no.…”

“…Bayesian clustering of SNP data was performed to infer homogeneous genetic clusters with STRUCTURE 2.3.4 ( Pritchard et al, 2000 ). Input datasets were generated by the snipStrup pipeline [available online at: https://github.com/MarekSlenker/snipStrup ; described in detail in Melichárková et al (2020) ]. This pipeline uses target sequences (those used for probe synthesis) as a reference and calls variants with respect to ploidy.…”