Interspecific introgression mediates adaptation to whole genome duplication

Abstract

Adaptive gene flow is a consequential evolutionary phenomenon across all kingdoms of life.While recognition of widespread gene flow is growing, examples lack of bidirectional gene flow mediating adaptations at specific loci that cooperatively manage core cellular processes.We previously described concerted molecular changes among physically interacting members of the meiotic machinery controlling crossover number and distribution upon adaptation to whole genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that escape from extinction following the trauma of WGD was mediated by adaptive gene flow between A. arenosa and its congener Arabidopsis lyrata. We show that A. lyrata underwent WGD more recently than A. arenosa, indicating that specific pre-adapted alleles donated by A. arenosa underwent selection and rescued the nascent A. lyrata tetraploids from early extinction. At the same time, we detect specific signals of gene flow in the opposite direction at other functionally interacting gene coding loci that display dramatic signatures of selective sweep in both tetraploid species. Cytological analysis shows that A. lyrata tetraploids exhibit similar levels of meiotic stability as A. arenosa tetraploids. Taken together, these data indicate that bidirectional gene flow allowed for an escape from extinction of the young autopolyploids, especially the rare tetraploid A. lyrata, and suggest that the merger of these species is greater than the sum of their parts.

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…10) and the absolute number of de-novo originated variants was low across all divergence levels. This corresponds to predictions about a substantial amount of shared variation between related species with high genetic diversity 33 and frequent adaptive trans-specific polymorphism in Arabidopsis 11,[45][46][47] . Absence of interspecific parallelism from gene flow was in line with the lack of genome-wide signal of recent migration between A. arenosa and A. halleri inferred by coalescent simulations ( Supplementary Fig.…”

Signatures of Introgression across the Allele Frequency Spectrum

“…As expected, D FS is skewed toward the lowest frequency variants and absolute values are low, consistent with a recent onset of inter-breeding ( Figure 5A). Tetraploid populations of Arabidopsis lyrata and A. arenosa are thought to have begun to hybridise extensively only after the emergence of tetraploid A. lyrata, around 80,000 generations ago (Marburger et al 2019). D FS is again skewed toward low frequencies but shows a much stronger signal than in the sparrows ( Figure 5B), consistent with a higher rate of recent gene flow.…”

“…Arabidopsis genotype data (Marburger et al 2019) were obtained from the authors. Only genotypes supported by an individual read depth ≥ 5 were considered, and sites genotyped in fewer than 80% of individuals were excluded.…”

“…The continued growth of genome-scale sequencing data now allows not only the detection of introgression, but also analysis of the fate of introgressed alleles. Such analyses provide insights into the timing of admixture events (Liu et al 2014), the role of adaptive introgression (Racimo et al 2017;Marburger et al 2019) and the nature of species boundaries (Aeschbacher et al 2017;Martin et al 2019).…”

Signatures of introgression across the allele frequency spectrum

“…Tetraploid populations of Arabidopsis lyrata and A. arenosa are thought to have begun to hybridise extensively only after the emergence of tetraploid A. lyrata, around 80,000 generations ago (Marburger et al 2019). D FS is again skewed toward low frequencies but shows a much stronger signal than in the sparrows ( Figure 5B), consistent with a higher rate of recent gene flow.…”