Multiple colonizations, hybridization and uneven diversification in Cyrtandra (Gesneriaceae) lineages on Hawai'i Island

International audienceAim The diversity and composition of species pools within oceanic archipelagos is determined by a combination of colonization, abiotic tolerance, in situ diversification, biotic interactions and extinction. The signature of biogeographic events and evolutionary processes, however, may be masked by recent coalescence and hybridization between closely related species. We used the species-rich plant genus Cyrtandra (Gesneriaceae) to investigate the roles of colonization and hybridization in shaping community assemblages on the geologically young Hawai'i Island. Location Hawaiian Islands. Taxon Cyrtandra (Gesneriaceae). Methods We sampled 29 Cyrtandra taxa and putative hybrids across the main Hawaiian Islands and generated single nucleotide polymorphisms (SNPs) from nine single-copy nuclear genes. Maximum likelihood and Bayesian inference were used to reconstruct phylogenetic relationships, divergence times were estimated using secondary calibrations and island ages, and ancestral area estimation was done using likelihood models. Lastly, we used a Bayesian population assignment test and principal components analysis to infer population genetic structure. Results Cyrtandra colonization of the main Hawaiian Islands appears to have followed the progression rule, whereby the oldest high Hawaiian Islands (Kaua'i and O'ahu) were colonized first, followed by colonization of the younger islands as habitat became available. Hawai'i Island was colonized four times, with two dispersal events from O'ahu and two from Maui Nui. The different colonization events gave rise to significantly uneven numbers of species, and hybridization among the incipient lineages was detected in the form of intermediate genotypes. Main conclusions Our investigation into community assembly in a species-rich plant genus on a geologically young oceanic island revealed a history of multiple colonizations and hybridization among colonizing lineages. The rapid diversification (3.5 species/My) of one of four Cyrtandra lineages on Hawai'i Island may be the result of hybridization between genetically diverse lineages that stem from independent colonization events. Multiple colonization events followed by a merging of lineages may be particularly common during early-stage community assembly on islands and, through the generation of genetic variation, may be especially important for species diversification