Northern glacial refugia and altitudinal niche divergence shape genome‐wide differentiation in the emerging plant model Arabidopsis arenosa

Abstract

Quaternary climatic oscillations profoundly impacted temperate biodiversity. For many diverse yet undersampled areas, however, the consequences of this impact are still poorly known. In Europe, particular uncertainty surrounds the role of Balkans, a major hotspot of European diversity, in postglacial recolonization of more northerly areas, and the Carpathians, a debatable candidate for a northern 'cryptic' glacial refugium. Using genome-wide SNPs and microsatellites, we examined how the interplay of historical processes and niche shifts structured genetic diversity of diploid Arabidopsis arenosa, a little-known member of the plant model genus that occupies a wide niche range from sea level to alpine peaks across eastern temperate Europe. While the northern Balkans hosted one isolated endemic lineage, most of the genetic diversity was concentrated further north in the Pannonian Basin and the Carpathians, where it likely survived the last glaciation in northern refugia. Finally, a distinct postglacial environment in northern Europe was colonized by populations of admixed origin from the two Carpathian lineages. Niche differentiation along altitude-related bioclimatic gradients was the main trend in the phylogeny of A. arenosa. The most prominent niche shifts, however, characterized genetically only slightly divergent populations that expanded into narrowly defined alpine and northern coastal postglacial environments. Our study highlights the role of eastern central European mountains not only as refugia for unique temperate diversity but also sources for postglacial expansion into novel high-altitude and high-latitude niches. Knowledge of distinct genetic substructure of diploid A. arenosa also opens new opportunities for follow-up studies of this emerging model of evolutionary biology.

Biogeography of the Carpathians: evolutionary and spatial facets of biodiversity

“…In plants, the herb Arabidopsis arenosa (Brassicaceae) provides an interesting recent example of the contribution of Carpathian lineages to northwards colonization of formerly glaciated areas. The Western Carpathians are generally considered as an important refugium and a central area for the evolution of this taxon (Schmickl et al ., ; Kolář, Fuxová et al ., ; Kolář, Lučanová et al ., 2016 ) and it is likely that the northernmost disjunct and ecologically distinct populations of diploid A. arenosa on the southern Baltic coast originated in the Holocene from admixture between Western and South‐Eastern Carpathian lineages (Kolář, Fuxová et al ., ).…”

“…Some of these studies are focused uniquely on the Carpathians, whereas others have a broader geographical context but also include an insight into Carpathian biogeography. These recent studies include herbaceous plants (Ronikier et al ., ; Stachurska‐Swakoń, Cieślak & Ronikier, ; Băcilă, Şuteu & Coldea, ; Pachschwöll et al ., ; György, Vouillamoz & Höhn, ; Kolář, Fuxová et al ., ; Wasowicz et al ., ), trees (Dzialuk et al ., ; Gömöry et al ., ; Lendvay et al ., ), invertebrates (Homburg et al ., ; Krascsenitsová et al ., ; Theissinger et al ., ; Kaňuch et al ., ; Schmitt et al ., ; Drees et al ., ), vertebrates (Fijarczyk et al ., ; McDevitt et al ., ; Zieliński et al ., ; Klinga et al ., ; Stojak et al ., ; Wielstra, Babik & Arntzen, ), and even microbial communities (Geremia et al ., ).…”

“…Kolář, Fuxová et al . () highlight an example of ecologically highly divergent (high‐mountain vs. low‐altitude) units that are not accompanied by significant genetic divergence. Molecular data in the geographical context are important for determining relationships in taxonomically intricate groups (Ujvárosi et al ., ; Meleg et al ., ; Copilaş‐Ciocianu & Petrusek, ) or genera undergoing extensive reticulate evolution, such as Aconitum (Ranunculaceae) (Sutkowska, Boroń & Mitka, ; Mitka et al ., , ).…”

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

“…Diploid A. lyrata colonized central and northern Europe as well as northern America, whereas the tetraploid form is limited to eastern Austria (15). For A. arenosa, the diploids are mainly found in the Carpathians and southeastern Europe, whereas the tetraploids occupy central and northern Europe (15,18,19). Diploid A. lyrata and A. arenosa are considered "good species" because they are genetically and phenotypically distinct and no past or recent gene flow can be detected between them (15,16).…”

Diverse paths to hybrid incompatibility in Arabidopsis

“…For the sequenced A. thaliana accessions, transcriptome and epigenome resources are also publically available (Kawakatsu et al ., ; http://neomorph.salk.edu/1001.aj.php). In addition to these resources, SNP genotyping using the restriction site associated DNA sequencing (RADseq) technique, allowing high‐density single‐nucleotide polymorphism (SNP) genotyping of thousands of individuals in a cost‐effective way (Davey et al ., ; Arnold et al ., ), has been applied to several species in the Arabidopsis genus (Todesco et al ., ; Buckley et al ., ; Jiang et al ., ; Kolář et al ., ; Fischer et al ., ; Swiadek et al ., ; Fan et al ., ). These genetic resources have not only improved the power of genome‐wide association (GWA) studies and quantitative trait locus (QTL) mapping, which are used to identify genes underlying adaptive traits in plants, but they have also allowed the study of evolution by comparison and analysis of genome sequences within and between individuals of the same and closely related species.…”