Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution

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.

FIG. 1.

Maps of seasonal synchrony and RST 1 strain prevalence. (A) Seasonal synchrony, measured as the area of overlap of immature tick seasonal host seeking activity curves, mapped by site. Large circles are sites characterized by a high degree of seasonal synchrony of immature tick stage activity, and small circles represent sites with little seasonal overlap. Data are divided into categories by quantiles. Background shading corresponds to the amplitude of the annual cycle of maximum temperature in degrees Celsius. Warm colors represent regions with extreme annual temperature cycles, while areas shaded with cooler colors are characterized by milder seasonal climates. (B) RST 1 strain infection prevalence in B. burgdorferi-positive ticks, mapped by site. Larger circles represent sites with high rates of RST 1 strain infection, while smaller circles indicate sites with low RST 1 strain prevalence in infected ticks. Data are divided into categories by quantiles. Map background shading is as described for panel A.

FIG. 2.

Seasonal activity of larvae and nymphs. Seasonal activity curves of immature tick host seeking based on 2-week moving averages of larval (solid lines/blue shading) and nymphal (dashed lines/red shading) host seeking. Observations of seasonal activity were pooled into two groups divided at the median of the seasonal synchrony index. Fifth-order polynomial trend lines were fitted for illustration purposes and are shown in black.

FIG. 3.

Relationship between seasonal synchrony and climate. Linear regression plot of the relationship between the area of overlap of immature tick seasonal host seeking activity curves and the amplitude of the annual cycle of maximum temperature. Solid gray line represents regression prediction. Dashed gray lines show the 95% confidence interval for the prediction line.

FIG. 4.

Relationships between RST 1 strain prevalence, climate, and seasonal synchrony. Logistic regression plot showing relationship between proportions of ticks infected with RST 1 strains and the amplitude of the annual cycle of maximum temperature (A) or seasonal synchrony measured as the area of overlap of immature tick seasonal host seeking activity curves (B). Circles are proportional to sample size. Solid gray lines are predicted probabilities of RST 1 strain infection. Dashed gray lines show 95% confidence intervals for predictions.