Single Geographic Origin of a Widespread Autotetraploid Arabidopsis arenosa Lineage Followed by Interploidy Admixture

Abstract

Whole-genome duplication, which leads to polyploidy, has been implicated in speciation and biological novelty. In plants, many species exhibit ploidy variation, which is likely representative of an early stage in the evolution of polyploid lineages. To understand the evolution of such multiploidy systems, we must address questions such as whether polyploid lineage(s) had a single or multiple origins, whether admixture occurs between ploidies, and the timescale over which ploidy variation affects the evolution of populations. Here we analyze three genomic data sets using nonparametric and parametric analyses, including coalescent-based methods, to study the evolutionary history of a geographically widespread autotetraploid variant of Arabidopsis arenosa, a new model system for understanding the molecular basis of autopolyploid evolution. Autotetraploid A. arenosa populations are widely distributed across much of Northern and Central Europe, whereas diploids occur in Eastern Europe and along the southern Baltic coast; the two ploidies overlap in the Carpathian Mountains. We find that the widespread autotetraploid populations we sampled likely arose from a single ancestral population approximately 11,000-30,000 generations ago in the Northern Carpathians, where its closest extant diploid relatives are found today. Afterward, the tetraploid population split into at least four major lineages that colonized much of Europe. Reconstructions of population history suggest that substantial interploidy admixture occurred in both directions, but only among geographically proximal populations. We find two cases in which selection likely acted on an introgressed locus, suggesting that persistent interploidy gene flow has a local influence on patterns of genetic variation in A. arenosa.

Borrowed alleles and convergence in serpentine adaptation

“…1B), consistent with ref. 12, but is most closely related to Hochlantsch in a simple phylogenetic analysis (SI Appendix, Section S1 and Table S2). This finding confirms that Gulsen is a member of the alpine lineage of A. arenosa and that, of all populations sampled across the A. arenosa range, the geographically most proximal populations (Hochlantsch and Kasparstein) provide the most closely related nonserpentine populations to Gulsen.…”

“…Because we detected hints of admixture between the Gulsen population of A. arenosa and A. lyrata, we included an Austrian A. lyrata genome sequence (from ref. 12) as an outgroup to quantify possible interspecies gene flow. With these three populations and five possible migration parameters (including migration between Gulsen, Hochlantsch, and A. lyrata) (SI Appendix, Table S4), we used a model selection approach (22) to determine which of these migration parameters were statistically supported by the data and thus potentially biologically meaningful.…”

“…Within the molecularly tractable Arabidopsis genus, at least two species have been reported to have independently colonized serpentine barrens: diploid Arabidopsis lyrata (7) and autotetraploid Arabidopsis arenosa. As an obligate outcrosser, A. arenosa exhibits very high genetic diversity, a small (∼200 Mb) genome, and very large effective population sizes (8,9), enabling fruitful population genomic analysis (9)(10)(11)(12). Tetraploid A. arenosa populations have colonized diverse habitats throughout central and northern Europe (13,14).…”

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

“…Moreover, the triploid hybrid is often either non-viable (triploid block) or unfit (Ramsey and Schemske, 1998;Köhler et al, 2010). Indeed, the few available empirical genetic studies document either much stronger (in autopolyploid systems : Ståhlberg, 2009;Jørgensen et al, 2011;Arnold et al, 2015) or exclusively unidirectional gene flow from the diploid into the polyploid (in allopolyploid systems: Slotte et al, 2008;Chapman and Abbott, 2010;Zohren et al, 2016). In a longer evolutionary timespan recurrent origins of autopolyploid lineages from different diploid sources followed by hybridization among these polyploids (Soltis and Soltis, 2009) would also lead to enrichment of the tetraploid gene pool by alleles from distinct diploid lineages, similar to direct unidirectional gene flow from diploid to polyploid.…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…In A. arenosa, tetraploids have been predicted to have arisen through autopolyploidisation (Arnold et al, 2015); secondary contact with A. lyrata during interglacial and postglacial range contractions and expansions has subsequently led to introgression between tetraploids in the two species. Our intent was to use investigation of S-receptor kinase evolution in this species complex as a model for understanding how balancing selection operates in polyploid genomes and to determine whether these highly polymorphic gene families could be useful indicators of hybridization and introgression.…”