Coinfections in ixodes scapularis from white-tailed deer compared to questing ixodes infer facultative mutualism across sites in Maryland, USA

Authors: MILHOLLAND, MATTHEW - University Of Maryland; XU, GUANG - University Of Massachusetts; RICH, STEPHEN - University Of Massachusetts; MACHTINGER, ERIKA - Pennsylvania State University; MULLINAX, JENNIFER - University Of Maryland; Li, Andrew

Submitted to: Vector-Borne and Zoonotic Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2020
Publication Date: 1/28/2021
Citation: Milholland, M.T., Xu, G., Rich, S.M., Machtinger, E.T., Mullinax, J.M., Li, A.Y. 2021. Coinfections in ixodes scapularis from white-tailed deer compared to questing ixodes infer facultative mutualism across sites in Maryland, USA. Vector-Borne and Zoonotic Diseases. https://doi.org/10.1089/vbz.2020.2644.
DOI: https://doi.org/10.1089/vbz.2020.2644

Interpretive Summary: The black-legged tick is responsible for transmitting pathogens that cause Lyme disease and other tick-borne diseases in humans in the United State. In addition to the pathogen that causes Lyme disease, ticks can also acquire several other tick-borne pathogens from their vertebrate hosts, particularly the white-footed mouse and white-trailed deer. There is little understanding of interaction among different pathogens in the vector and how that may affect disease transmission. To better understand the disease ecology and pathogen-vector interactions that affects pathogen transmission, the USDA-ARS scientists led a team of investigators from several universities to address the knowledge gap. Unfed and fed adult ticks were collected from tick habitats and white-tailed deer, respectively. Key tick-borne pathogens in individual ticks were identified using PCR techniques. This study indicated the prevalence of the three major pathogens in adult ticks differed proportionally between sites and among feeding and questing ticks. These differences suggested adult ticks may benefit through facultative relationships offered by co-infections with these pathogens. Results obtained from this study are of interest to tick-borne disease epidemiologists, tick biologists, and researchers who work in the field of vector control and integrated pest management.

Technical Abstract: The steady increase of tick-borne pathogens (TBPs) is of global concern and poses great risk to human and animal health. Most TBPs are zoonotic, shaped by anthropogenic interruptions to natural host-pathogen ecology. Pervasive landscape alterations have created discontinuous patches of limited green spaces throughout urban settings resulting in more frequent human-wildlife encounters. Urban habitats are favorable to generalist species such as the White-tailed deer (Odocoileus virginianus). These ungulates are important hosts to Ixodes scapularis that transmit agents of Lyme Borreliosis. At field sites in central Maryland, we found consistent coinfections of Anaplasma phagocytophilum and B. burgdorferi (sensu lato) in ticks from deer, and strong associations of B. burgdorferi and Babesia microti in questing ticks. Each of these pathogens are known to have evolutionary strategies to manipulate tick immune defenses which can facilitate pathogen persistence and maintenance in the environment. We sampled eight sites across central Maryland collecting Ixodes ticks using drag-cloths and retrieved others from deer carcasses. Pathogen species in each tick were determined using qPCR. We collected a total of 889 ticks (n=571, deer, n=318, questing) that revealed landscape level prevalence of A. phagocytophilum (50%), B. burgdorferi (25%), and B. microti (2.9%). Prevalence differed proportionally between sites and among feeding and questing ticks. These differences suggested adult Ixodes ticks may benefit through facultative relationships offered by coinfections with these pathogens.