Parental legacy, demography, and admixture influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae)

Abstract

Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species nor how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe, and the Middle East. We phased the two subgenomes, one descended from the outcrossing and highly diverse Capsella grandiflora ( Cbp Cg ) and the other one from the selfing and genetically depauperate Capsella orientalis ( Cbp Co ). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size ( N e ), signatures of positive and negative selection, and gene expression patterns. In all three regions, N e of the two subgenomes decreased gradually over time and the Cbp Co subgenome accumulated more deleterious changes than Cbp Cg . There were signs of widespread admixture between C. bursa-pastoris and its diploid relatives. The two subgenomes were impacted differentially depending on geographic region suggesting either strong interploidy gene flow or multiple origins of C. bursa-pastoris . Selective sweeps were more common on the Cbp Cg subgenome in Europe and the Middle East, and on the Cbp Co subgenome in Asia. In contrast, differences in expression were limited with the Cbp Cg subgenome slightly more expressed than Cbp Co in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence, the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy but their evolutionary trajectory strongly varied across geographic regions.

Shift in ecological strategy helps marginal populations of shepherd's purse (Capsella bursa-pastoris) to overcome a high genetic load

“…Furthermore, as expected given the species history, the East Asian populations (i.e. colonization front) presented a reduced genetic diversity and a higher amount of deleterious mutations than the European and Middle Eastern ones (core populations) [15].…”

“…Cbp probably first occurred in the Middle East (ME), then spread to Europe (EU) before invading eastern Asia (AS) and more recently spread worldwide as a result of human migrations [13]. Owing to limited gene flow between these geographic areas, three main genetic clusters can be delineated from both nuclear DNA and gene expression data [13,15,16]. Furthermore, as expected given the species history, the East Asian populations (i.e.…”

“…Both A. thaliana and C. rubella reference partition databases were used to classify the single nucleotide polymorphisms (SNPs). To get only the annotation of the mutations that occurred after speciation of Cbp, the mutations with reconstructed ancestral sequences were polarized as in Kryvokhyzha et al [15] and only derived mutations were analysed. This was done for the two subgenomes of Cbp the one derived from C. grandiflora and the one derived from C. orientalis, leading to two estimates of the proportion of deleterious mutations, μ delCg and μ delCo , respectively.…”

“…Here, we conducted an experiment under controlled environmental conditions following the whole life cycle of Cbp accessions whose number of potentially deleterious mutations had been estimated from whole genome sequence data [15]. Life-history traits, fertility, viability of the progeny, phenological traits (germination time, flowering start) and vegetative traits (growth of the rosette) were assessed in Cbp accessions coming from the three main genetic clusters.…”

Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus

“…This finding agrees with theoretical work of transcription factor binding and regulatory mismatch that predicts increasing subgenome dominance over generations in newly established allopolyploids (16) . Preexisting differences between parental genomes has been shown to influence observed subgenome dynamics in an allopolyploid (17,18) . For example, analyses of diverse allopolyploids have revealed that gene expression differences among subgenomes mirrors differences in transposable element (TE) densities in flanking regions surrounding genes (12,19,20) .…”