Evolution of the distribution area of the Mediterranean Nigella damascena and a likely multiple molecular origin of its perianth dimorphism

Abstract

Nigella damascena (Ranunculaceae) is a common Mediterranean species traditionally used as condiment and healing herb. Its perianth dimorphism has been known since 1591. In all modern accessions examined to date, a single allele of the NdAP3–3 gene characterized by a MITE insertion has been found to be responsible for the mutant morph, lacking a corolla. Based on herbarium collections, we aimed at (i) reconstructing the evolution of the worldwide distribution area of both morphs of N. damascena, and (ii) assessing the diversity in the molecular origin of the mutant allele.We compiled a database of more than 3000 collections of N. damascena across four centuries. When possible, specimens were georeferenced, and distribution maps were built for the wild-type and mutant morphs. Additionally, we genotyped the NdAP3–3 locus, based on DNA extracted from herbarium specimens collected from various localities and at different times.We observe a consistently larger and denser distribution area of wild-type plants in Europe and North Africa compared with the mutant morph. The relative proportions of mutant and wild-type morph plants collected in the last couple of centuries are roughly similar. Interestingly in herbarium specimens, NdAP3–3 alleles without a MITE insertion can be found in plants exhibiting the mutant morph.The diachronic study of the distribution area of N. damascena and a literature survey showed that populations exhibiting the mutant phenotype have been present since the end of the 16th century, though not frequently, in the broad Mediterranean Basin. Our genotyping results indicate that the origin of the mutant morph may be multiple and suggest that the NdAP3–3 allele with the MITE insertion typically found in all modern accessions to date, is only a sample of the variability susceptible to disrupt petal formation and development in Nigella damascena.