Phylogenomics of the sigmodontine rodents: Cloud forests and Pliocene extinction explain timing and spread of the radiation of South American mice and rats

Studies of radiations after invasion often overlook the potential role of climatic, biotic, and geologic triggers, instead focusing largely on the conduit for invasion. For example, studies of the rodent subfamily Sigmodontinae, a clade of over 500 species that radiated throughout South America during the Great American Biotic Interchange, have historically focused more on invasion than potential triggers or subsequent environmental change. Here, we put the timing and transitions of this radiation in context of changing climatic, biotic, and geologic factors by reconstructing the biogeography of the radiation. To accomplish this, we generated the largest genomic phylogeny of Sigmodontinae that include over 80% of the genera and 40% of the known species, including all incertae sedis taxa and produced a fossil-calibrated chronogram. Results indicate a single invasion of South America at the base of Sigmodontinae (∼ 10.46 million years ago [mya]) with two waves of increased lineage generation and biogeographic transition rates, the first of which occurred after a four-million-year lag following invasion. The timing and location of this initial radiation (6.61 - 5.78 mya) coincided with the spread of montane cloud forest during the Late Miocene Cooling and sigmodontines did not spread throughout the continent until the Mid-Pliocene Faunal Turnover (4.5 – 3.0 mya), a period of high extinction of South American mammals. A comprehensive classification for the subfamily is provided that accounts for the new results.