The blacklegged tick, Ixodes scapularis (Acari: Ixodidae), is the vector of Borrelia burgdorferi, the causal agent of Lyme disease (LD) in the eastern United States. Ninety-five per cent of LD cases are reported from the Northeast and upper Midwest, despite the widespread presence of the vector throughout the South. Several hypotheses have been proposed to explain this difference in disease risk. These include geographic variation in large-scale factors such as climatic variables, biodiversity, and tick genetics, which are known and/or believed to influence the abundance of infected ticks in an area. While these factors may explain the ultimate causes of risk variation, they do not reveal the proximate underlying mechanisms maintaining the geographic discrepancy in disease risk. In this dissertation, I propose and demonstrate that a mechanistic factor - the questing behavior of nymphs (the epidemiologically most important life stage of the vector) - is a key factor explaining this gradient in LD risk. I hypothesized that variation in questing behavior is such that nymphs from low LD risk areas (southern regions) rarely host-seek in locations where they come into contact with human hosts, whereas nymphs from high LD risk areas (northern regions) host-seek in locations where human encounters are more likely. I addressed the following specific hypotheses via a 4-year series of field experiments at sites located within the current distribution of I. scapularis:H1: Nymphal I. scapularis host-seeking behavior varies with geographic origin (Chapter 1); H2: Behavioral differences exhibited by nymphs from different geographic origins are maintained when nymphs are translocated to other regions (Chapter 1);H3: The broad geographic variation in human LD risk is strongly correlated with geographic variation in nymphal questing behavior (Chapter 2);H4: The hybrid offspring of I. scapularis from high- and low-risk regions will differ in questing behavior from one or both parental populations (Chapter 3).In Chapter 1, using outdoor experimental behavior arenas placed at four sites in the eastern US, I demonstrate that nymphal blacklegged ticks derived from a LD-endemic (northern) region were 3.6-11.6 times more likely to be observed questing than were nymphs from non-endemic (southern) regions. Furthermore, the observed behavior trends of northern and southern nymphs were consistent in both years and at all sites where they were tested, implicating a genetic component for questing behavior. In Chapter 2, I confirm the generality of the trends observed in Chapter 1 by using the same experimental approach to observe questing behavior of I. scapularis nymphs originating from 15 locations throughout the eastern US. The results of these experiments were consistent with those of Chapter 1; I found that nymphs from LD-endemic regions were much up to 8 times as likely to emerge from underneath the leaf litter versus those from non-endemic regions, regardless of the field site where they were tested. Furthermore, questing behavior was strongly positively related to the LD incidence of the region from which the nymph’s mothers were collected which provides further support for the role of questing behavior and human LD risk. In Chapter 3, I explored potential consequences of I. scapularis range expansion by mating northern and southern tick and found that hybrid ticks behave more like southern nymphs, but with enhanced survival. Future studies on I. scapularis reproductive behavior and biology are necessary to better understanding how local ecology will influence LD risk in areas where northern and southern populations meet.
Read
