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.

Correlation of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks with Specific Abiotic Traits in the Western Palearctic

“…Previous reports of higher prevalence in eastern Europe seem to be the result of studies examining small numbers of ticks, which may be adequate for the local assessment of the presence of B. burgdorferi sensu lato but unsatisfactory for the appraisal of prevalence patterns in a wide area. One of the most relevant results of our study was the relationship between abiotic traits and the prevalence of B. burgdorferi sensu lato in nymphal ticks, uncovering a relationship between prevalence and temperature already suggested in previous studies (14,26). Thus, environmental features of the Western Palearctic region are linked to the geographic pattern of variation in B. burgdorferi sensu lato prevalence in ticks.…”

“…Recently, OspA serotype 4 of B. garinii has been associated with a new species, Borrelia bavariensis (30). Some studies have indicated the influence of tick life cycle traits on the distribution of B. burgdorferi sensu stricto genotypes in the United States as a consequence of different climate patterns affecting tick phenology (14). A temperatureregulated pattern of B. burgdorferi sensu stricto genotypes in the United States has been interpreted as the control of the synchrony of the activity of the different tick stages by the yearly temperature amplitude and persistence of the pathogen in the primary reservoir host (14).…”

“…Some studies have indicated the influence of tick life cycle traits on the distribution of B. burgdorferi sensu stricto genotypes in the United States as a consequence of different climate patterns affecting tick phenology (14). A temperatureregulated pattern of B. burgdorferi sensu stricto genotypes in the United States has been interpreted as the control of the synchrony of the activity of the different tick stages by the yearly temperature amplitude and persistence of the pathogen in the primary reservoir host (14). The abundance of ticks is determined not only by climate cues but also by the extrinsic incubation period of spirochetes in ixodid ticks, which equals the duration of development from larva to nymph and is climate sensitive (35).…”

Phylogeography of Borrelia burgdorferi in the eastern United States reflects multiple independent Lyme disease emergence events

“…However, transport of B. burgdorferi between northeastern and midwestern I. scapularis populations appears to be relatively infrequent. Regional isolation of B. burgdorferi genotypes may have epidemiological implications due to differences in clinical outcomes associated with specific genotypes (51)(52)(53)(54)(55).…”

Host-Seeking Phenology ofIxodes pacificus(Acari: Ixodidae) Nymphs in Northwestern California in Relation to Calendar Week, Woodland Type, and Weather Conditions

“…Previous studies in North America have shown that the host-seeking phenologies of the primary vectors of Lyme disease spirochetes-the nymphal stages of Ixodes scapularis Say in the east and Ixodes pacificus Cooley and Kohls in the far west-are strongly associated with environmental variables (Lane et al 1995;Vail and Smith 1998;Eisen et al 2002Eisen et al , 2003Eisen et al , 2016Diuk-Wasser et al 2006;Gatewood et al 2009). …”