Multiple Autopolyploid Arabidopsis lyrata Populations Stabilized by Long-Range Adaptive Introgression Across Eurasia

Abstract

Abundance of established polyploid lineages varies across lineages, evolutionary time, and geography, suggesting both genetics and environment play a role in polyploid persistence. We show Arabidopsis lyrata is the most polyploid-rich species complex in the Arabidopsis genus, with multiple origins of autotetraploidy. This is revealed by genomic data from over 400 A. lyrata samples across Eurasia. We found over 30 previously undescribed autotetraploid populations in Siberia with a minimum of two separate origins, independent of those previously reported in Central Europe. The establishment of Siberian tetraploids is mediated by meiotic adaptation at the same genes as in European tetraploid A. lyrata and Arabidopsis arenosa, despite their genomic divergence and geographical separation. Haplotype analysis based on synthetic long-read assemblies supports the long-range introgression of adaptive alleles from the tetraploid interspecific pool of European A. lyrata and A. arenosa to tetraploid Siberian A. lyrata. Once adaptations to polyploidy emerge, they promote the establishment of new polyploid lineages through adaptive inter- and intraspecific introgression.

Keywords: Arabidopsis lyrata; adaptation; introgression; polyploid.

Fig. 1.

Distribution of diploid and tetraploid A. lyrata across Eurasia. a) Geographical distribution of A. lyrata samples used in this study. For better visualization in cases of overlaps we randomly shifted the points within 100 km from the actual sampling location, all true coordinates can be found in the supplementary data S1, Supplementary Material online. Newly found tetraploid A. lyrata populations are represented in orange circles. b) Relationships between proportions of heterozygous biallelic SNPs and the number of different S-alleles in each individual shown in (a). Tetraploid individuals (orange dots) show a higher proportion of heterozygous sites and up to four different S-alleles. Diploid individuals (blue dots) show a lower proportion of heterozygous sites and up to two different S-alleles; individuals with one S-allele below the dashed gray line correspond to recently described Siberian selfing A. lyrata lineage with nonfunctional S-locus (Kolesnikova et al. 2023). Herbarium individuals with ambiguous assignments of ploidy between two inference methods are shown in gray dots.

Fig. 2.

Population structure of A. lyrata diploid-tetraploid species complex. a) Network representation of genetic pairwise distances (Nei's D) between individuals. Arabidopsis lyrata accessions form several clusters outside of Central Europe, named here as NU (pink, diploid/tetraploid), WS (blue, diploid), CS (yellow, diploid/tetraploid), ES (orange, diploid), and Amur Basin (AB; turquoise, diploid). Note that while network clusters may contain multiple ploidy levels, geographic populations are not mixed ploidy. Newly described autotetraploids are found in two distinct clusters (NU/pink and CS/yellow), distinct from Central European autotetraploids (gray), and allotetraploid A. kamchatica. b) ASTRAL summary phylogeny of 4,000 gene trees from stLFR assemblies of A. lyrata and PacBio assemblies of A. arenosa, with A. thaliana as outgroup. Each tip is an accession, shape reflects taxon (square = A. lyrata, circle = A. arenosa) and color denotes ploidy (blue = diploid, orange = tetraploid). Thicker branches have a quartet support of 1.00. Branch lengths reported in coalescent units. Dotted branch subtending the outgroup has been shortened for easier plotting. Color of each clade is consistent with labeling in (a). c) Admixture across the Eurasian A. lyrata distribution. Colors correspond to labeling in (a) and (b) and reflect average admixture proportions per sampling site. Tetraploid accessions are found across the range (denoted by black outlines). Extent of the ice sheet during the LGM (Ehlers et al. 2011) shown in white.

Fig. 3.

Genes present in introgression topologies. a) Map showing tetraploid lineages as circles, Grey = Central Europe, Pink = Northern Ural, Yellow = Central Siberian. Each plot is a distribution of introgression topology windows along a chromosome, with upper panels (black) showing introgression windows between NU and CS tetraploids, and lower panels (gray) showing introgression windows between Central Europe and NU tetraploids. Height of peaks indicates topology weighting, and introgression blocks are annotated. Blocks may contain multiple gene models, see supplementary data S4, Supplementary Material online for full list. Red dashed line indicates 50% weight. b to d) gene trees for haplotypes from A. lyrata in Siberia, A. lyrata in Central Europe, and A. arenosa. Each tip is a haplotype, orange tips are haplotypes from tetraploid individuals, and blue tips from diploids. Shape indicates taxon: squares for A. lyrata in Siberia, diamonds for A. lyrata in Central Europe, and circles for A. arenosa. Orange box highlights derived tetraploid haplotype clade (b) Haplotype tree for PDS5b (c) Haplotype tree for ASY3 (d) Haplotype tree for ZYP1b.