Fifty million years of beetle evolution along the Antarctic Polar Front

Significance The Antarctic environment is famously inhospitable to most terrestrial biodiversity, traditionally viewed as a driver of species extinction. Combining population- and species-level molecular data, we show that beetles on islands along the Antarctic Polar Front diversified in response to major climatic events over the last 50 Ma in surprising synchrony with the region’s marine organisms. Unique algae- and moss-feeding habits enabled beetles to capitalize on cooling conditions, which resulted in a decline in flowering plants—the typical hosts for beetles elsewhere. Antarctica’s cooling paleoclimate thus fostered the diversification of both terrestrial and marine life. Climatically driven evolutionary processes since the Miocene may underpin much of the region’s diversity, are still ongoing, and should be further investigated among Antarctic biota. Global cooling and glacial–interglacial cycles since Antarctica’s isolation have been responsible for the diversification of the region’s marine fauna. By contrast, these same Earth system processes are thought to have played little role terrestrially, other than driving widespread extinctions. Here, we show that on islands along the Antarctic Polar Front, paleoclimatic processes have been key to diversification of one of the world’s most geographically isolated and unique groups of herbivorous beetles—Ectemnorhinini weevils. Combining phylogenomic, phylogenetic, and phylogeographic approaches, we demonstrate that these weevils colonized the sub-Antarctic islands from Africa at least 50 Ma ago and repeatedly dispersed among them. As the climate cooled from the mid-Miocene, diversification of the beetles accelerated, resulting in two species-rich clades. One of these clades specialized to feed on cryptogams, typical of the polar habitats that came to prevail under Miocene conditions yet remarkable as a food source for any beetle. This clade’s most unusual representative is a marine weevil currently undergoing further speciation. The other clade retained the more common weevil habit of feeding on angiosperms, which likely survived glaciation in isolated refugia. Diversification of Ectemnorhinini weevils occurred in synchrony with many other Antarctic radiations, including penguins and notothenioid fishes, and coincided with major environmental changes. Our results thus indicate that geo-climatically driven diversification has progressed similarly for Antarctic marine and terrestrial organisms since the Miocene, potentially constituting a general biodiversity paradigm that should be sought broadly for the region’s taxa.