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Abstract Genital morphology, a cornerstone in taxonomy that predates Linnaeus’s Systema Naturae, is vital for species delimitation. However, the widely accepted paradigm that genitalia are taxonomically informative lacks robust testing between closely related species, and supporting evidence is often limited to taxonomic literature in which genitalia are assumed a priori to be species-specific. The cosmopolitan ant genus Nylanderia Emery includes 123 described species, with most in the Neotropics still undescribed. Workers are often morphologically cryptic, and males are rare in collections but required for morphological delimitation. Using Ultraconserved Elements (UCEs) from 236 samples, including 53 Neotropical Nylanderia species, we reconstructed a phylogenetic framework to compare the genitalia (gonopods) of males collected alongside workers. We used geometric morphometrics on images of slide-mounted genitalia from 16 species and nano-CT scans of Nylanderia fulva (Mayr) and Nylanderia pubens (Forel) genital capsules and interpreted results considering phylogeny under maximum likelihood and the multispecies coalescent. We found strong morphological and molecular support for 2 distantly related American clades, identifiable by gonopod shape, with significant differences observed among most species. Three previously reported COI clades of N. fulva were not supported as monophyletic, nor were their gonopods significantly different. However, N. pubens was supported as distinct by all phylogenetic and 3DGM results. Our findings emphasize the importance of male genitalia for delimiting species boundaries and revising Neotropical Nylanderia. Given their importance, particularly in morphologically cryptic taxa, we recommend a greater focus on linking male and worker phenotypes, which can be facilitated through comprehensive nest series collection. 

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.