Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self-compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae (Arabidopsis suecica, Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S-locus from one parental lineage was dominant over the functional S-locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.

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A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here we explain how self-compatibility evolved in diploid SiberianArabidopsis lyrata, and how it contributed to the establishment of allotetraploidA. kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploidA. lyrataaccessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in SiberianA. lyrata, date this independent transition to ~90 Kya, and infer evolutionary relationships between Siberian and North AmericanA. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing SiberianA. lyratalineage contributed to the formation of the allotetraploidA. kamchaticaand propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited fromA. lyrata.

A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here, we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid Arabidopsis kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to ∼90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

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