The blacklegged tick, Ixodes scapularis, is a vector of Borrelia burgdorferi sensu stricto (s.s.), the causative agent of Lyme disease, part of a slow-moving epidemic of Lyme borreliosis spreading across the northern hemisphere. There are well-known geographic differences in the vectorial capacity of these ticks associated with genetic variation. Despite the need for detailed genetic information in this disease system, previous phylogeographic studies of these ticks have been restricted to relatively few populations or genetic loci. Here we present the most comprehensive phylogeographic study of I. scapularis conducted by using 3RAD and surveying 353 ticks from 33 counties throughout the range of I. scapularis. We found limited genetic variation among populations from the Northeast and Upper Midwest, where Lyme disease is most common, and higher genetic variation among populations from the South. We identify four genetic clusters of I. scapularis that are consistent with four major geographic regions, plus a distinct Central Florida group. In regions where Lyme disease is increasing in frequency, the I. scapularis populations genetically group with ticks from historically highly Lyme-endemic regions. Finally, we identify ten variable DNA sites that contribute the most to population differentiation. These variable sites cluster on one of the chromosome-scale scaffolds for I. scapularis and are within identified genes. Our findings illuminate the need for additional research to identify loci causing variation in the vectorial capacity of I. scapularis and where additional tick sampling would be most valuable to further understand disease trends caused by pathogens transmitted by I. scapularis.
