Diversification and Biogeography of North American Thistles (Cirsium: Carduoideae: Compositae): Drivers of a Rapid Continent-Wide Radiation

Premise of research. Cirsium (“thistles”), the most speciose genus in the Compositae (Asteraceae) subfamily Carduoideae native to North America, comprises a rapid endemic radiation. Hummingbird pollination is rare in Compositae, but approximately 10% of all Cirsium in North America are adapted to this pollination syndrome. Although Cirsium is an example of a continent-wide evolutionary radiation, the biotic and abiotic factors contributing to this remarkable diversification have never been studied. Methodology. Sixty-four taxa of Cirsium representing its distribution in North America were sequenced using the MYbaits Compositae 1061 1kv1 kit. These results were used to infer a time-calibrated phylogeny to estimate divergence times and diversification rates. Ancestral area reconstructions for eight biogeographical areas and 10 habitats were performed with BioGeoBEARS. A model-fitting approach was used to test whether (1) different environmental variables were related to diversification, (2) pollinator type was related to differences in environment, and (3) pollinator type was related to diversification. Phylogenetic least squares models against diversification rates were used to test whether environmental variables, pollinator type, or morphological traits influenced diversification. Pivotal results. Cirsium in North America originated approximately 2 mya, with the majority of the diversification occurring in three nearly simultaneous bursts during the onset of the Pleistocene ice age. Although most traits showed evidence of phylogenetic signal, there were no significant morphological innovations that contributed to overall diversification in Cirsium. Precipitation and semiaridity were the main catalysts for diversification. Hummingbird pollination was associated with near-significant lower rates of diversification than insect pollination. Conclusions. The integrated effects of niche conservatism and glacial-interglacial cycles played a role in shaping current distributional patterns, particularly in alpine mountain systems and canyons of the Colorado Plateau. Although hummingbird pollination was associated with lower rates of diversification in Cirsium, the switch to this syndrome may have facilitated expansion across post-Pleistocene fragmented landscapes. Ultimately, this study offers important insights into the drivers of a rapid, continent-wide radiation and the impact of Pleistocene glaciation cycles on the flora of North America.