| Abstract: | The blacklegged tick, Ixodes scapularis, is of significant public health importance as a vector of Borrelia burgdorferi, the agent of Lyme borreliosis. The timing of seasonal activity of each immature I. scapularis life stage relative to the next is critical for the maintenance of B. burgdorferi because larvae must feed after an infected nymph to efficiently acquire the infection from reservoir hosts. Recent studies have shown that some strains of B. burgdorferi do not persist in the primary reservoir host for more than a few weeks, thereby shortening the window of opportunity between nymphal and larval feeding that sustains their enzootic maintenance. We tested the hypothesis that climate is predictive of geographic variation in the seasonal activity of I. scapularis, which in turn differentially influences the distribution of B. burgdorferi genotypes within the geographic range of I. scapularis. We analyzed the relationships between climate, seasonal activity of I. scapularis, and B. burgdorferi genotype frequency in 30 geographically diverse sites in the northeastern and midwestern United States. We found that the magnitude of the difference between summer and winter daily temperature maximums was positively correlated with the degree of seasonal synchrony of the two immature stages of I. scapularis. Genotyping revealed an enrichment of 16S-23S rRNA intergenic spacer restriction fragment length polymorphism sequence type 1 strains relative to others at sites with lower seasonal synchrony. We conclude that climate-associated variability in the timing of I. scapularis host seeking contributes to geographic heterogeneities in the frequencies of B. burgdorferi genotypes, with potential consequences for Lyme borreliosis morbidity.An increasingly important area of research in infectious disease epidemiology is the influence of pathogen strain diversity on patterns of disease risk and clinical outcome. Strain-specific pathogenicity or transmissibility can be important clinical and epidemiological parameters; for example, only a subset of Neisseria meningitidis strains are responsible for invasive infections leading to meningitis (1). Geography and environmental features influence the genetic structure of certain pathogens by regulating their distribution, dispersal, or population size (8, 31, 49). Accordingly, a heterogeneous environment will result in spatial structuring of genotype frequencies, with possible epidemiological implications.Lyme borreliosis is a tick-borne zoonosis caused by Borrelia burgdorferi, a spirochetal bacterium that exhibits genetic diversity throughout its range in eastern North America (12, 60), where it is maintained in a horizontal transmission cycle between its vector, the blacklegged tick Ixodes scapularis, and vertebrate reservoir hosts. I. scapularis has a two-year life cycle in which it takes three blood meals, one per life stage, with the two subadult stages responsible for the enzootic maintenance of B. burgdorferi (2, 3, 51). Larval ticks hatch uninfected from eggs (41) and acquire the spirochetes from infected reservoir hosts. Infected larvae maintain the spirochetes transstadially, allowing them to transmit B. burgdorferi to uninfected reservoirs during their nymphal blood meal the following summer. The seasonal timing of activity, or phenology, of each tick life stage relative to the next is a critical factor in the maintenance of B. burgdorferi because larvae typically must feed after an infected nymph in order to acquire the bacteria (32).Previous studies in Europe of tick-borne encephalitis virus have shown that seasonal synchrony of immature ticks is necessary for the maintenance of the virus in natural enzootic cycles because nonsystemic infections are transmitted from nymphs to larvae feeding in close proximity on the same individual reservoir rodent (48). Furthermore, seasonal synchrony of immature tick activity, a prerequisite of cofeeding, was found to be correlated with climate (47). Although it is possible for an I. scapularis larva to become infected with B. burgdorferi by simultaneously feeding in close proximity to an infected nymph, a role for cofeeding transmission in the enzootic maintenance of B. burgdorferi in North America has not been established (43). Rather, until recently, the existing evidence indicated that B. burgdorferi causes life-long systemic infections in reservoirs that allow for its maintenance in the absence of seasonal synchrony of I. scapularis immatures (18). However, recent studies suggest that this may not always be the case (34) and that there are differences in the duration of infectiousness that are strain specific (16, 28).We hypothesized that large-scale, climate-driven geographic variability in the host seeking phenology of immature I. scapularis ticks is associated with heterogeneity in the frequencies of strains acquired by larval ticks. Using regression models and accounting for spatial autocorrelation, we examined the relationships between climate, the temporal synchrony of larval and nymphal seasonal host seeking activity, and B. burgdorferi genotype frequency in ticks collected from 30 geographically diverse sites systematically selected for their locations throughout the northeastern and midwestern United States.Here we present empirical evidence that climate patterns, specifically, regional variation in summer and winter temperature cycle extremes, are associated with variation in the seasonal synchrony of I. scapularis larval and nymphal host seeking activity. Furthermore, both climate and the differences in the seasonal synchrony of the two immature tick stages are related to geographic variation in B. burgdorferi genotype frequency. Our results point to the impact of climate upon the natural dynamics of enzootic transmission and population genetic structure of an important vector-borne human pathogen, with possible implications for the distribution of human disease risk and epidemiology. |
