Out of the Andes and up to the Arctic: multiple drivers promote rapid radiation in Colias butterflies

The drivers of insect radiation in mountain ecosystems are poorly understood compared to birds and plants. The drivers of insect radiation in mountain ecosystems are poorly understood compared to birds and plants. We studied the rapid radiation of the butterfly genus Colias, which has diversified in mountain ecosystems in Eurasia, Africa, and the Americas. Based on a dataset of 150 nuclear protein-coding genetic loci and whole mitochondrial genomes, we constructed a time-calibrated tree of the genus Colias with broad taxon sampling. We then inferred historical characteristics of this genus, including ancestral range reconstruction, historical diversification rates, and the evolution of host plant use. We found that rapid diversification was driven by several factors including favorably warm climates in the mid-Pliocene that promoted the population expansion, and the formation of the Isthmus of Panama and the Bering Land Bridge, which led to intercontinental dispersals that opened new ecological opportunities. These two extrinsic factors may simultaneously be the main extrinsic drivers of the genus' rapid diversification. Introgression may have improved the ecological adaptability of the genus Colias, and we propose that this is the primary intrinsic driver of diversification. Expansion of host plant breadth enabling population expansion was a secondary driving factor. We suggest that mountain uplift had little effect on the diversity of Colias after the initial split from the common ancestor shared with its sister taxon Zerene and emphasize the importance of historical climatic and geological events for studies of rapid radiations of montane species.