Highlights d Six high-quality ixodid tick genomes and 678 re-sequenced tick specimens d Insights into the genetic basis of tick hematophagy and related phenotypes d Population structure and genetic diversity of six tick species d Tick-borne pathogen composition and distribution by metagenome analyses

Background Haemaphysalis longicornis, a vector of various pathogens with medical and veterinary importance, is native to eastern Asia, and recently reached the USA as an emerging disease threat. In this study, we aimed to identify the geographical distribution, hosts, and associated pathogens of H longicornis.Methods Data were collected from multiple sources, including a field survey, reference book, literature review, and related websites. The thematic maps showing geographical distribution of H longicornis and associated pathogens were produced by ArcGIS. Hosts of H longicornis and positive rates for H longicornis-associated pathogens were estimated by meta-analysis. Ecological niche modelling was used to predict potential global distribution of H longicornis.Findings H longicornis was found to be present in ten countries, predominantly in eastern Asia, the USA, Australia, and New Zealand. The tick was known to feed on a variety of domestic and wild animals, and humans. At least 30 human pathogens were associated with H longicornis, including seven species of spotted fever group rickettsiae, seven species in the family of Anaplasmataceae, four genospecies in the complex Borrelia burgdorferi sensu lato, two Babesia species, six species of virus, and Francisella, Bartonella, Coxiella, and Toxoplasma, which were mainly reported in eastern Asia. The predictive modelling revealed that H longicornis might affect more extensive regions, including Europe, South America, and Africa, where the tick has never been recorded before.Interpretation H longicornis is relatively common in the world, and is associated with various human and animal pathogens. Authorities and health-care workers should be aware of the threat of the tick species to public health and veterinary medicine. Surveillance and further investigations should be enhanced globally.

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The increasing prevalence and expanding distribution of tick-borne viruses globally have raised health concerns, but the full repertoire of the tick virome has not been assessed. We sequenced the meta-transcriptomes of 31 different tick species in the Ixodidae and Argasidae families from across mainland China, and identified 724 RNA viruses with distinctive virome compositions among genera. A total of 1,801 assembled and complete or nearly complete viral genomes revealed an extensive diversity of genome architectures of tick-associated viruses, highlighting ticks as a reservoir of RNA viruses. We examined the phylogenies of different virus families to investigate virome evolution and found that the most diverse tick-associated viruses are positive-strand RNA virus families that demonstrate more ancient divergence than other arboviruses. Tick-specific viruses are often associated with only a few tick species, whereas virus clades that can infect vertebrates are found in a wider range of tick species. We hypothesize that tick viruses can exhibit both ‘specialist’ and ‘generalist’ evolutionary trends. We hope that our virome dataset will enable much-needed research on vertebrate-pathogenic tick-associated viruses.

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