Cytogenetic insights into an oceanic island radiation: The dramatic evolution of pre-existing traits in Cheirolophus (Asteraceae: Cardueae: Centaureinae)

Abstract

The genus Cheirolophus constitutes one of the most striking cases of species radiation in Macaronesia, where it diversified into a lineage of ca. 20 endemic species at a rate that is amongst the fastest reported for oceanic islands. Whilst the cytogenetic dynamics of many of the Macaronesian Cheirolophus species have been comparatively well studied, an overall vision of chromosome and genome evolution has been hampered by the lack of data for the earliestdiverging species, Ch. crassifolius. In this study, we have completed the cytogenetic survey of Cheirolophus to investigate how different cytogenetic traits may have contributed to the dramatic radiation of the genus in Macaronesia. We provide new cytogenetic data (i.e., chromosome counts, genome size estimates and physical mapping of 35S rDNA loci) for several key species, including Ch. crassifolius, and then model trait evolution within a phylogenetic context. Our results reveal a trend of genome downsizing accompanied by a dramatic increase in number of 35S rDNA loci which started early in the evolutionary history of the genus, before its radiation in Macaronesia. It is notable that the increasing number of 35S rDNA loci has not been driven by polyploidisation, in contrast to the more typical trend observed in many angiosperms. In addition, the number of 35S rDNA loci was observed to negatively correlate with genome size, which is also very unusual in angiosperms. It is suggested that nonhomologous and unequal homologous recombination are the most likely mechanisms to explain these observations and we discuss whether the unique genomic architectures of Cheirolophus could have predisposed the genus to its successful and rapid speciation in Macaronesia.