When clades collide: Genomic admixture in blacklegged ticks (Ixodes scapularis) from the Great Plains

Ixodes scapularis ticks transmit a number of pathogens important to human health, including Borrelia burgdorferi, the causative agent of Lyme disease. While I. scapularis is found across the Eastern United States, Lyme disease transmission is largely limited to the Northeast and Upper Midwest and is nearly absent in the South. This indicates that differences in northern versus southern clades of I. scapularis are associated with differences in Lyme disease transmission risk. I. scapularis is undergoing range expansion, including into the Great Plains region of the United States. Determining where I. scapularis populations in the Great Plains originated can inform future risk of Lyme disease transmission in this region. In this study, we use a population genomics framework to characterize diversity, structure, and B. burgdorferi infection rates of I. scapularis populations in the Great Plains region. We generated whole genome sequence data and single nucleotide polymorphism (SNP) datasets from I. scapularis ticks collected in Iowa, Kansas, Nebraska, and South Dakota to compare to publicly available data from across the species range. Our analysis of 200 I. scapularis SNP datasets indicated geographically well-defined populations that correspond to historical northern and southern ancestral clades of I. scapularis. Ticks from South Dakota, Iowa, and northeastern Nebraska are genetically similar populations from the Upper Midwest, while ticks from Kansas are more genetically similar to ticks from the Southeast. Ticks collected in the central eastern region of Nebraska, however, represent an evenly admixed population of both northern and southern genomic backgrounds. Analysis of B. burgdorferi reads from genomic datasets shows [~]50% infection rate in ticks from Iowa and northeastern Nebraska, whereas ticks from Kansas show no evidence of B. burgdorferi infection. Of note, evenly admixed ticks from the central eastern region of Nebraska also show no evidence of B. burgdorferi infection. These results provide further evidence that tick genomics may influence traits associated with B. burgdorferi infection status, and thus the potential for Lyme disease transmission. As the range of I. scapularis continues to expand, bringing historically isolated populations into contact, there is a clear need to understand the consequence of genomic admixture for B. burgdorferi transmission potential to inform future risk of Lyme disease in the United States.