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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.

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