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

Andrea Melichárková,Karol Marhold,Marek Svitok,Tatiana Kačmárová,Matúš Kempa,Lenka Mártonfiová,Martin A Lysák,Katarína Skokanová,Barbora Šingliarová,Judita Zozomová-Lihová,Gabriela Šrámková,Terezie Mandáková,Marek Šlenker,Michaela Caboňová

doi:10.3389/fpls.2020.588856

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.

Highlights

Polyploidy is a widespread evolutionary phenomenon and a major mechanism of sympatric speciation in plants (Soltis et al, 2003; Coyne and Orr, 2004; Soltis and Soltis, 2009; Soltis et al, 2014)
We sampled all species recognized in Central Europe, and representatively covered their geographic, elevational and cytotypic variation (Figure 1 and Supplementary Data 1)
C. rivularis growing in Southeastern Europe was sampled and analyzed here for proper interpretation of the highelevation Central European populations previously attributed to this species (Table 1), as well as due to its hybridization with C. matthioli reported by Ancev et al (2013, see below)

Summary

Introduction

Polyploidy is a widespread evolutionary phenomenon and a major mechanism of sympatric speciation in plants (Soltis et al, 2003; Coyne and Orr, 2004; Soltis and Soltis, 2009; Soltis et al, 2014). Recurrent polyploid formation and weak reproductive barriers between cytotypes or polyploid lineages generate intricate polyploid species complexes with reticulate evolutionary histories (e.g., Bardy et al, 2010; Ma et al, 2010; Frajman et al, 2016; Španiel et al, 2017; Mandák et al, 2018; Padilla-García et al, 2018; Melichárková et al, 2019). They frequently show weak genetic separation among polyploid species, discrepancies between morphological and genetic patterns, and shallow, largely unresolved phylogenetic structuring. Understanding the evolutionary processes that generated the present-day variation patterns, cytotypic and genetic structure in European polyploid species complexes is a challenging task

Objectives

Methods

Results

Conclusion