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Interspecific hybridization is an important evolutionary force promoting plant speciation. In the genus Onosma, one of three main evolutionary lineages presumably evolved by hybrid speciation. The assumed hybrid lineage (Heterotricha) consists of two species complexes with bimodal karyotypes containing different numbers of large ( L) and small ( S) chromosomes, the tetraploid Onosma pseudoarenaria (2 n = 12 L + 14S) and the triploid Onosma arenaria (2 n = 12 L + 8S). The latter represents a rare case of hemisexual, asymmetrically compensating allopolyploids. Representatives of the other two lineages of the genus, Haplotricha (2 n = 12 L) and Asterotricha (2 n = 14S), have been considered to be the ancestral taxa of O. pseudoarenaria and O. arenaria, although this has yet to be investigated critically. In the present study, we examined genetic [amplified fragment length polymorphism ( AFLP), internal transcribed spacer ( ITS) , and chloroplast (cp) DNA)], reproductive (pollen viability and seed production) and cytogenetic (chromosome counts, genome size assessment) patterns to resolve the hypothesized allopolyploid formations in the Heterotricha group, single or polytopic allopolyploid origins, as well as ongoing interspecific gene flow as one piece of evidence for understanding past hybrid speciation events in the genus. Discordant patterns in maternally inherited cp DNA ( Heterotricha accessions bearing the haplotypes related to asterotrichous species) and the nuclear ITS and AFLP markers ( Heterotricha clustering with haplotrichous Onosma fastigiata), as well as karyological features, support the hybrid origin of the stabilized Heterotricha lineage. Genetic variation that is both large and geographically correlated indicates multiple origins of Heterotricha allopolyploids or, less likely, a single origin with recurring introgression from the progenitor species. The nuclear markers and cytogenetic features also provide evidence for the ongoing hybridization between O. arenaria and Onosma echioides (2 n = 14S), which gives rise to sterile triploids of 2 n = 6 L + 15S. We contrast the two cases of triploids with LLS (hemisexual O. arenaria from the stabilized Heterotricha lineage) and LSS (recent sterile hybrids) karyotypes, which could help to understand the mechanisms ensuring the establishment and reproductive fitness of the odd allopolyploids in Onosma. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 89-107. [ABSTRACT FROM AUTHOR]