The twisted-winged parasite genus Stylops has a history of different species concepts with varying host specificity resulting in diverse species diversity estimates in different regions of the Holarctic. The adoption of a supergeneralist species concept in Europe, proposing synonymization of all Western Palaearctic Stylops species, did not facilitate taxonomic clarity and obscured the available life-history data in the region for decades. Lack of molecular data has allowed divergent opinions on species hypotheses and little opportunity for evaluating them in this morphologically challenging genus. To solve these discrepancies and gain novel information about host associations, we applied whole-genome sequencing to 163 specimens, representing a significant portion of putative European species. We evaluate the existing and conflicting species hypotheses with molecular species delimitation using Species bOundry Delimitation using Astral (SODA) and use a maximum likelihood phylogeny to investigate host associations of the species. Furthermore, we evaluate the effect of a number of loci used in SODA for the number of inferred species. We find justification for synonymization of multiple species and indications of undescribed species, as well as new host–parasite relationships. We show that the number of inferred species in SODA is exceedingly and positively correlated with the number of loci used, urging for cautious application. The results of our study bring clarity to the Western Palaearctic species diversity of Stylops. Furthermore, the comprehensive molecular dataset generated in this study will be a valuable resource for future studies on Stylops and the evolution of parasites in general. 

Holarctic Stylops is the largest genus of the enigmatic insect order Strepsiptera, twisted winged parasites. Members of Stylops are obligate endoparasites of Andrena mining bees and exhibit extreme sexual dimorphism typical of Strepsiptera. So far, molecular studies on Stylops have focused on questions on species delimitation. Here, we utilize the power of whole genome sequencing to infer the phylogeny of this morphologically challenging genus from thousands of loci. We use a species tree method, concatenated maximum likelihood analysis and Bayesian analysis with a relaxed clock model to reconstruct the phylogeny of 46 Stylops species, estimate divergence times, evaluate topological consistency across methods and infer the root position. Furthermore, the biogeographical history and coevolutionary patterns with host species are assessed. All methods recovered a well resolved topology with close to all nodes maximally supported and only a handful of minor topological variations. Based on the result, we find that included species can be divided into 12 species groups, seven of them including only Palaearctic species, three Nearctic and two were geographically mixed. We find a strongly supported root position between a clade formed by the spreta, thwaitesi and gwynanae species groups and the remaining species and that the sister group of Stylops is Eurystylops or Eurystylops + Kinzelbachus. Our results indicate that Stylops originated in the Western Palaearctic or Western Palaearctic and Nearctic in the early Neogene or late Paleogene, with four independent dispersal events to the Nearctic. Cophylogenetic analyses indicate that the diversification of Stylops has been shaped by both significant coevolution with the mining bee hosts and host-shifting. The well resolved and strongly supported phylogeny will provide a valuable phylogenetic basis for further studies into the fascinating world of Strepsipterans.