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Fungus-farming ants cultivate multiple lineages of fungi for food, but, because fungal cultivar relationships are largely unresolved, the history of fungus-ant coevolution remains poorly known. We designed probes targeting >2000 gene regions to generate a dated evolutionary tree for 475 fungi and combined it with a similarly generated tree for 276 ants. We found that fungus-ant agriculture originated ~66 million years ago when the end-of-Cretaceous asteroid impact temporarily interrupted photosynthesis, causing global mass extinctions but favoring the proliferation of fungi. Subsequently, ~27 million years ago, one ancestral fungal cultivar population became domesticated, i.e., obligately mutualistic, when seasonally dry habitats expanded in South America, likely isolating the cultivar population from its free-living, wet forest–dwelling conspecifics. By revealing these and other major transitions in fungus-ant coevolution, our results clarify the historical processes that shaped a model system for nonhuman agriculture. 

Abstract Nylanderia(Emery) is one of the world's most diverse ant genera, with 123 described species worldwide and hundreds more undescribed. Fifteen globetrotting or invasive species have widespread distributions and are often encountered outside their native ranges. A molecular approach to understanding the evolutionary history and to revision ofNylanderiataxonomy is needed because historical efforts based on morphology have proven insufficient to define major lineages and delimit species boundaries, especially where adventive species are concerned. To address these problems, we generated the first genus‐wide genomic dataset ofNylanderiausing ultraconserved elements (UCEs) to resolve the phylogeny of major lineages, determine the age and origin of the genus, and describe global biogeographical patterns. Sampling from seven biogeographical regions revealed a Southeast Asian origin ofNylanderiain the mid‐Eocene and four distinct biogeographical clades in the Nearctic, the Neotropics, the Afrotropics/Malagasy region, and Australasia. The Nearctic and Neotropical clades are distantly related, indicating two separate dispersal events to the Americas between the late Oligocene and early Miocene. We also addressed the problem of misidentification that has characterized species‐level taxonomy inNylanderiaas a result of limited morphological variation in the worker caste by evaluating the integrity of species boundaries in six of the most widespreadNylanderiaspecies. We sampled across ranges of species in theN. bourbonicacomplex (N. bourbonica(Forel) + N. vaga(Forel)), theN. fulvacomplex (N. fulva(Mayr) + N. pubens(Forel)), and theN. guatemalensiscomplex (N. guatemalensis(Forel) + N. steinheili(Forel)) to clarify their phylogenetic placement. Deep splits within these complexes suggest that some species names – specificallyN. bourbonicaandN. guatemalensis– each are applied to multiple cryptic species. In exhaustively samplingNylanderiadiversity in the West Indies, a ‘hot spot’ for invasive taxa, we found five adventive species among 22 in the region; many remain morphologically indistinguishable from one another, despite being distantly related. We stress that overcoming the taxonomic impediment through the use of molecular phylogeny and revisionary study is essential for conservation and invasive species management.