The Insurgence of Strong Hybrid Seed Inviability Explains the Initial Phases of Divergence in the Rapidly Evolving Dianthus rupicola Complex

Abstract

Understanding the mechanisms underlying fast diversifications is central to evolutionary biology. This can be partly achieved by focusing on intrinsic reproductive barriers that emerge during early stages of divergence in fast‐radiating groups. Here, we explored the mechanisms underlying the divergence of two ecotypes of the Dianthus rupicola complex, which belong to the Eurasian clade of the hyperdiverse genus Dianthus , the fastest reported radiation among angiosperms. We combined phenotypic and genomic analyses, reciprocal crosses, and micromorphological observations at different stages of seed development (i.e., 3, 6, and 9 days after pollination) to discover putative reproductive barriers between these ecotypes. Our findings indicate that the ecotypes started diverging approximately 87 kya and rapidly developed strong hybrid seed inviability. Consistent with a divergence in Endosperm Balance Number (EBN) between the ecotypes, we observed a parent‐of‐origin growth effect on hybrid seeds which led to asymmetric seed size in reciprocal crosses. Genomic analyses revealed low levels of admixture between the two ecotypes despite their recent origin, consistent with the presence of strong intrinsic barriers to gene flow. This admixture was explained by past introgression rather than recent hybridization between the ecotypes. Overall, our study highlights the primary role of hybrid seed inviability in maintaining reproductive isolation in a rapid evolutionary radiation. Moreover, it opens new avenues for dissecting the molecular basis and the eventual ecological drivers of endosperm‐mediated incompatibilities, as well as their largely unexplored yet potentially decisive contribution to diversification at short evolutionary timescales.

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