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Impact of polymorphic transposable elements on linkage disequilibrium along chromosomes

Choudhury, Rimjhim Roy, Rogivue, Aude, Gugerli, Felix, Parisod, Christian
Molecular ecology 2019 v.28 no.6 pp. 1550-1562
Arabis alpina, cold, flowering, genes, genetic variation, haplotypes, linkage disequilibrium, loci, outcrossing, photoperiodism, salt stress, sequence analysis, transposons
Recombination and selection drive the extent of linkage disequilibrium (LD) among loci and therefore affect the reshuffling of adaptive genetic variation. However, it is poorly known to what extent the enrichment of transposable elements (TEs) in recombinationally‐inert regions reflects their inefficient removal by purifying selection and whether the presence of polymorphic TEs can modify the local recombination rate. In this study, we investigate how TEs and recombination interact at fine scale along chromosomes and possibly support linked selection in natural populations. Whole‐genome sequencing data of 304 individuals from nearby alpine populations of Arabis alpina were used to show that the density of polymorphic TEs is specifically correlated with local LD along chromosomes. Consistent with TEs modifying recombination, the characterization of 28 such LD blocks of up to 5.5 Mb in length revealed strong evidence of selective sweeps at a few loci through either site frequency spectrum or haplotype structure. A majority of these blocks were enriched in genes related to ecologically relevant functions such as responses to cold, salt stress or photoperiodism. In particular, the S‐locus (i.e., supergene responsible for strict outcrossing) was identified in a LD block with high levels of polymorphic TEs and evidence of selection. Another such LD block was enriched in cold‐responding genes and presented evidence of adaptive loci related to photoperiodism and flowering being increasingly linked by polymorphic TEs. These results are consistent with the hypothesis that TEs modify recombination landscapes and thus interact with selection in driving blocks of linked adaptive loci in natural populations.