Abstract
Hosts including humans, other vertebrates, and arthropods, are frequently infected with heterogeneous populations of pathogens. Within-host pathogen diversity has major implications for human health, epidemiology, and pathogen evolution. However, pathogen diversity within-hosts is difficult to characterize and little is known about the levels and sources of within-host diversity maintained in natural populations of disease vectors. Here, we examine genomic variation of the Lyme disease bacteria, Borrelia burgdorferi (Bb), in 98 individual field-collected tick vectors as a model for study of within-host processes. Deep population sequencing reveals extensive and previously undocumented levels of Bb variation: the majority (~70%) of ticks harbor mixed strain infections, which we define as levels Bb diversity pre-existing in a diverse inoculum. Within-tick diversity is thus a sample of the variation present within vertebrate hosts. Within individual ticks, we detect signatures of positive selection. Genes most commonly under positive selection across ticks include those involved in dissemination in vertebrate hosts and evasion of the vertebrate immune complement. By focusing on tick-borne Bb, we show that vectors can serve as epidemiological and evolutionary sentinels: within-vector pathogen diversity can be a useful and unbiased way to survey circulating pathogen diversity and identify evolutionary processes occurring in natural transmission cycles.
Highlights
Hosts including humans, other vertebrates, and arthropods, are frequently co-infected with multiple pathogen species in addition to diverse populations of pathogens of the same species
Lyme disease, caused by a bacteria carried by deer ticks, is the most common vector-borne disease in North America and over 30,000 cases are reported each year in the United States
Ticks may be infected with multiple strains of the Lyme disease bacteria, which differ in transmissibility and the harm they pose to humans
Summary
Other vertebrates, and arthropods, are frequently co-infected with multiple pathogen species in addition to diverse populations of pathogens of the same species. Neutral and adaptive evolutionary processes acting on heterogeneous pathogen populations, including population bottlenecks occurring during the host’s infection and during transmission[8,9], selection within and between-hosts [9,10,11], and recombination between co-infecting strains[12] further shape patterns of pathogen diversity. Within-host diversity may arise from multiple independent infection events, pre-existing diversity in the inoculum, and in situ evolution. Distinguishing between these sources of diversity allows us to identify ecological and evolutionary processes occurring within-host (e.g. within-host competition of strains and/or host-imposed selection) or across hosts (e.g. transmission dynamics and/or population-level selection)[3]
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