Recent hybrid speciation at the origin of the narrow endemic Pulmonaria helvetica

Background and Aims Hybridization is known to drive plant speciation through the establishment of homoploid or allopolyploid hybrid species. Here we investigate the origin of Pulmonaria helvetica, a narrow endemic species described across a restricted area of Switzerland that was entirely covered by ice during the last glacial maximum. This species presents an original number of chromosomes (2n = 24) and morphological traits suggestive of a hybrid origin. Methods We sequenced a plastid locus and 1077 double-digest restriction-site-associated DNA (ddRAD) loci in 67 individuals from across the distribution range of P. helvetica and candidate progenitor species growing in the same area. Assignment of genotypes to main genetic clusters within and among taxa using STRUCTURE tested whether P. helvetica represents a genetically differentiated lineage and addressed the hypothesis of its hybrid origin. Comparative ecological modelling further addressed possible niche differentiation among taxa. Key Results Pulmonaria helvetica was highlighted as a genetically homogeneous species distinct from co-occurring taxa. Consistent with a scenario of hybrid speciation, it presented clear evidence of balanced admixture between Pulmonaria officinalis (2n = 16) and Pulmonaria mollis s.l. (2n = 18, 22), which was also highlighted as a maternal progenitor based on plastid sequences. Limited genetic structure within the maternal progenitor is consistent with an origin of P. helvetica through either homoploid hybridization with considerable karyotype changes or via complex scenarios of allopolyploidy involving a dysploid taxon of P. mollis s.l. Comparative niche modelling indicated non-significant ecological differences between P. helvetica and its progenitors, supporting intrinsic factors resulting from hybridization as main drivers of speciation. Conclusions Hybridization appears as a major process having promoted the postglacial origin of the narrow endemic P. helvetica, suggesting hybrid speciation as an effective process that rapidly produces new species under climate changes.

Automated summary

Genetic and ecological studies suggest that Pulmonaria helvetica may have originated from a hybridization event between Pulmonaria officinalis and Pulmonaria mollis s.l. Structural genetic analysis indicated balanced admixture with P. mollis s.l. as the maternal progenitor. Ecological niche modelling revealed non-significant differences between P. helvetica and its progenitors, supporting hybridization as the main driver of speciation in this case.