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.

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 and 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 (Cg) and the other one from the selfing and genetically depauperate Capsella orientalis (Co). For each subgenome, we assessed its relationship with the diploid relatives, temporal change of effective population size Ne, signatures of positive and negative selection, and gene expression patterns. Introgression between C. bursa-pastoris and its diploid relatives was widespread and the two subgenomes were impacted differentially depending on geographic region. In all three regions, Ne of the two subgenomes decreased gradually and the Co subgenome accumulated more deleterious changes than Cg. Selective sweeps were more common on the Cg subgenome in Europe and the Middle East, and on the Co subgenome in Asia. In contrast, differences in expression were limited with the Cg subgenome slightly more expressed than 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 and were differentially affected by introgression and selection.

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