Abstract
BackgroundUnderstanding the drivers of Lyme disease incidence at broad spatial scales is critical for predicting and mitigating human disease risk. Previous studies have identified vector phenology and behavior, host community composition, and landscape features as drivers of variable Lyme disease risk. However, while the Lyme disease transmission cycles in the eastern and western USA involve different vector species (Ixodes scapularis and Ixodes pacificus, respectively), the role of vector-specific differences in transmission efficiency has not been directly examined. By comparing the performance of traits involved in vector competence between these two species, this study aims to identify how vector competence contributes to variable Lyme disease risk.MethodsWe used a suite of laboratory experiments to compare the performance of traits related to vector competence for the two USA Lyme disease vectors. For each species, we measured the rate of attachment to a common rodent host, the engorgement weight, and the efficiency of pathogen acquisition (host to tick) and pathogen transmission (tick to host) from laboratory mice. In measuring pathogen acquisition and transmission, we used two different pathogen strains, one sympatric with I. scapularis and one sympatric with I. pacificus, to assess the importance of vector-pathogen coevolutionary history in transmission dynamics.ResultsWe found I. pacificus had significantly higher host attachment success and engorgement weights, but significantly lower pathogen transmission efficiency relative to I. scapularis. Molting success and pathogen acquisition did not differ between these two species. However, pathogen acquisition efficiency was significantly higher for both sympatric vector and pathogen strains than the allopatric pairings.ConclusionsThis study identified species-specific vector traits as a potential driver of broad scale variation in Lyme disease risk in the USA. In particular, the exceedingly low rates of pathogen transmission from tick to host observed for I. pacificus may limit Lyme disease transmission efficiency in the western USA. Further, observed variation in pathogen acquisition between sympatric and allopatric vector-pathogen strains indicate that vector-pathogen coevolutionary history may play a key role in transmission dynamics. These findings underscore the need to consider vector traits and vector-pathogen coevolution as important factors governing regional Lyme disease risk.
Highlights
Understanding the drivers of Lyme disease incidence at broad spatial scales is critical for predicting and mitigating human disease risk
Host attachment success and feeding time Of the 300 larvae of each tick species placed on P. maniculatus, 102 I. pacificus and 20 I. scapularis successfully attached and fed (Fig. 2)
Pathogen acquisition efficiency was identical between I. scapularis and I. pacificus for their respective allopatric strain, lower than that of their sympatric strain. These results indicate that I. scapularis and I. pacificus are capable of acquiring pathogens from infected hosts, and highlight the importance of coevolutionary history between vectors and pathogen strain in vector competence
Summary
Understanding the drivers of Lyme disease incidence at broad spatial scales is critical for predicting and mitigating human disease risk. Previous studies have identified vector phenology and behavior, host community composition, and landscape features as drivers of variable Lyme disease risk. While the Lyme disease transmission cycles in the eastern and western USA involve different vector species (Ixodes scapularis and Ixodes pacificus, respectively), the role of vector-specific differences in transmission efficiency has not been directly examined. The divergent Lyme disease cycles in the eastern and western USA present an ideal system for studying ecological drivers of human incidence at broad spatial scales. In the eastern USA, B. burgdorferi transmission is maintained by a suite of small mammal hosts, most notably white-footed mice, least chipmunks, long-tailed and short-tailed shrews and bushy-tailed squirrels; and transmitted between hosts by the blacklegged tick, Ixodes scapularis [13]. In the western USA, B. burgdorferi is maintained primarily by the western gray squirrel, dusky-footed woodrat and deer mice, and vectored by the western blacklegged tick, Ixodes pacificus [14]
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