Genome resequencing reveals population divergence and local adaptation of blacklegged ticks in the United States

Authors: SCHOVILLE, SEAN - University Of Wisconsin; DONG, DAHN-YOUNG - University Of Wisconsin; PASKEWITZ, SUSAN - University Of Wisconsin; Maestas, Lauren; TSAO, JEAN - Michigan State University; BURKE, RUSSELL - Hofstra University; GINSBERG, HOWARD - University Of Rhode Island

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2024
Publication Date: 7/4/2024
Citation: Schoville, S.D., Dong, D., Paskewitz, S., Maestas, L.P., Tsao, J., Burke, R.L., Ginsberg, H. 2024. Genome resequencing reveals population divergence and local adaptation of blacklegged ticks in the United States. Molecular Ecology. https://doi.org/10.1111/mec.17460.
DOI: https://doi.org/10.1111/mec.17460

Interpretive Summary: Tick vectors and tick-borne disease are increasingly impacting human populations globally. An important challenge is to understand tick movement patterns, as this information can be used to improve tick management and predictive modeling of tick population dynamics. Evolutionary analysis of genetic relatedness, gene flow, and local adaptation provides important insight on movement patterns at large scale and across time. We develop low coverage, whole genome resequencing data for 92 samples representing range-wide variation in blacklegged ticks, Ixodes scapularis, across the United States. Through analysis of population genetic makeup data, we find that tick populations are grouped by geography, with gradual genetic isolation by distance separating three population clusters in the northern U.S., southeastern U.S., and a unique cluster sampled from Tennessee. Populations in the northern U.S. underwent population restrictions during the last glacial period and grew apart from southern populations at least 50 thousand years ago. Genome scans of selection provide strong evidence of local adaptation at genes responding to host defenses, blood-feeding, and environmental variation. In addition, we explore the role of low coverage genome sequencing of whole-tick samples for documenting the diversity of pathogens. Large scale genetic analyses recover important tick-borne pathogens and their geographical variation, including the restriction of the bacteria that cause Lyme disease in northern tick populations, geographic strain variation in various other disease causing organisms. The combination of restricted pathogen distribution, isolation by distance, and local adaptation in blacklegged ticks demonstrates that movement, including recent expansion, has been limited to geographical scales of a few hundred kilometers.

Technical Abstract: Tick vectors and tick-borne disease are increasingly impacting human populations globally. An important challenge is to understand tick movement patterns, as this information can be used to improve tick management and predictive modeling of tick population dynamics. Evolutionary analysis of genetic divergence, gene flow, and local adaptation provides important insight on movement patterns at large spatial and temporal scales. We develop low coverage, whole genome resequencing data for 92 samples representing range-wide variation in blacklegged ticks, Ixodes scapularis, across the United States. Through analysis of population genomic data, we find that tick populations are structured geographically, with gradual isolation by distance separating three population clusters in the northern U.S., southeastern U.S., and a unique cluster sampled from Tennessee. Population in the northern U.S. underwent population contractions during the last glacial period and diverged from southern populations at least 50 thousand years ago. Genome scans of selection provide strong evidence of local adaptation at genes responding to host defenses, blood-feeding, and environmental variation. In addition, we explore the role of low coverage genome sequencing of whole-tick samples for documenting the diversity of microbial pathogens. Metagenomic analyses recover important tick-borne pathogens and their geographical variation, including the restriction of Borrelia burgdorferi to northern populations, geographic strain variation in Rickettsia species, and the rare occurrence of B. miyamotoi and Anaplasma phagocytophilum. The combination of restricted pathogen distribution, isolation by distance, and local adaptation in blacklegged ticks demonstrates that movement, including recent expansion, has been limited to geographical scales of a few hundred kilometers.