Genomic signatures of native (Japanese) and introduced (Oceanian) populations of the Asian longhorned tick Haemaphysalis longicornis

Abstract

Abstract The Asian longhorned tick (Haemaphysalis longicornis) impacts the health of humans, livestock, and wildlife, both as a parasite and a vector. Over more than a century, H. longicornis has become a widespread invasive species across much of the Asia-Pacific region, with a recent emergence in North America. This dispersal success could be associated with the ability of certain lineages of H. longicornis to reproduce via parthenogenesis. We analyzed complete mitochondrial genomes and genome-wide single-nucleotide polymorphisms (SNPs) from ticks collected within the native range of H. longicornis (Japan), invasive populations in the Asia-Pacific (Australia, Fiji, and New Caledonia), and laboratory-maintained parthenogenetic and bisexual strains. We also compared our data with DNA sequences in GenBank from invasive populations in other countries (e.g., United States). Two distinct clades (Mt-Clade 1 and Mt-Clade 2) were observed in the phylogenetic tree based on mitochondrial genomes. All specimens from the bisexual laboratory strains were assigned to Mt-Clade 1 and those from the parthenogenetic laboratory strains were assigned to Mt-Clade 2, whereas the field-collected male specimens were included in both clades. No geographical cline associated with the phylogenetic characteristics was observed. In contrast, analyses based on genome-wide SNPs demonstrated a cluster composed of Oceanian samples apart from Japanese samples and detected gene flow between the two mitogenomic clades. Our results suggest that parthenogenesis may have evolved multiple times within H. longicornis rather than originating from a single evolutionary event.