The range of hosts a pathogen can infect is a key trait, influencing human disease risk and reservoir host infection dynamics. Borrelia burgdorferi sensu stricto (Bb), an emerging zoonotic pathogen, causes Lyme disease and is widely considered a host generalist, commonly infecting mammals and birds. Yet the extent of intraspecific variation in Bb host breadth, its role in determining host competence, and potential implications for human infection remain unclear. We conducted a long-term study of Bb diversity, defined by the polymorphic ospC locus, across white-footed mice, passerine birds, and tick vectors, leveraging long-read amplicon sequencing. Our results reveal strong variation in host breadth across Bb genotypes, exposing a spectrum of genotype-specific host-adapted phenotypes. We found support for multiple niche polymorphism, maintaining Bb diversity in nature and little evidence of temporal shifts in genotype dominance, as would be expected under negative frequency-dependent selection. Passerine birds support the circulation of several human-invasive strains (HISs) in the local tick population and harbor greater Bb genotypic diversity compared with white-footed mice. Mouse-adapted Bb genotypes exhibited longer persistence in individual mice compared with nonadapted genotypes. Genotype communities infecting individual mice preferentially became dominated by mouse-adapted genotypes over time. We posit that intraspecific variation in Bb host breadth and adaptation helps maintain overall species fitness in response to transmission by a generalist vector.
This content will become publicly available on November 28, 2024
Disease ecologists commonly use abiotic factors (e.g. temperature and moisture) or measures of biodiversity (e.g. species richness) to predict Lyme disease transmission patterns, but variance in infection probability among individuals within a population is poorly understood. Most studies assume intraspecific consistency, but recent evidence suggests that individual traits, such as animal personality, may drive differences in encounter rates with infected vectors and pathogen transmission probabilities through differential space use and microhabitat selection, leading to intraspecific variation in infection probability. In addition, because vectors and hosts are nonrandomly distributed across a landscape, land-use changes that modify key habitat features—such as forest management practices—may substantially alter associations between individual traits and infection probability. To address these gaps in our knowledge, we used a large-scale capture–mark–recapture study targeting Peromyscus mice in Maine, United States, to test whether personality drives probability of Borrelia burgdorferi infection in hosts within managed forest compartments with different silvicultural treatments. Specifically, we tested effects of individual phenotypic traits (physical and behavioral) and environmental traits (microhabitat and forest type) on infection probability within 2 species: P. leucopus and P. maniculatus. We found evidence that boldness negatively influences infection probability in P. maniculatus, and that body mass positively influences infection probability in both species. We found no effect of mouse density, microhabitat, or forest type in our analyses. These results suggest that personalities vary in their functional contributions to the natural cycle of B. burgdorferi, and that broader integration of behavioral diversity in disease ecology studies may aid in identifying key transmission zones for this rapidly expanding vector-borne zoonosis.
more » « less- Award ID(s):
- 1940525
- NSF-PAR ID:
- 10484989
- Editor(s):
- Wang, Guiming
- Publisher / Repository:
- ASM
- Date Published:
- Journal Name:
- Journal of Mammalogy
- ISSN:
- 0022-2372
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
The range of hosts a pathogen can infect is a key trait influencing human disease risk and reservoir host infection dynamics. Borrelia burgdorferi sensu stricto (Bb), an emerging zoonotic pathogen, causes Lyme disease and is widely considered a host generalist, commonly infecting mammals and birds. Yet the extent of intraspecific variation in Bb host breadth, its role in determining host competence and potential implications to human infection remain unclear. We conducted a long-term study of Bb diversity, defined by the polymorphic ospC locus, across white-footed mice, passerine birds, and tick vectors leveraging long-read amplicon sequencing. Our results reveal strong variation in host breadth across Bb genotypes, exposing a spectrum of genotype-specific host-adapted phenotypes. We found support for multiple niche polymorphism maintaining Bb diversity in nature and little evidence of temporal shifts in genotype dominance, as would be expected under negative frequency-dependent selection. Passerine birds support the circulation of several human invasive strains in the local tick population and harbor greater Bb genotypic diversity compared to white-footed mice. Mouse-adapted Bb genotypes exhibited longer persistence in individual mice compared to non-adapted genotypes and infection communities infecting individual mice preferentially became dominated by mouse-adapted genotypes over time. We posit that intraspecific variation in Bb host breadth and specificity helps maintain overall species fitness in response to transmission by a generalist vector. Because pathogen genotypes vary in host breadth and result in diverse human disease manifestations, our findings indicate that a more nuanced definition of ‘host competence’ incorporating local genotype frequency is warranted.more » « less
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The range of hosts a pathogen can infect is a key trait influencing human disease risk and reservoir host infection dynamics. Borrelia burgdorferi sensu stricto (Bb), an emerging zoonotic pathogen, causes Lyme disease and is widely considered a host generalist, commonly infecting mammals and birds. Yet the extent of intraspecific variation in Bb host breadth, its role in determining host competence and potential implications to human infection remain unclear. We conducted a long-term study of Bb diversity, defined by the polymorphic ospC locus, across white-footed mice, passerine birds, and tick vectors leveraging long-read amplicon sequencing. Our results reveal strong variation in host breadth across Bb genotypes, exposing a spectrum of genotype-specific host-adapted phenotypes. We found support for multiple niche polymorphism maintaining Bb diversity in nature and little evidence of temporal shifts in genotype dominance, as would be expected under negative frequency-dependent selection. Passerine birds support the circulation of several human invasive strains in the local tick population and harbor greater Bb genotypic diversity compared to white-footed mice. Mouse-adapted Bb genotypes exhibited longer persistence in individual mice compared to non-adapted genotypes and infection communities infecting individual mice preferentially became dominated by mouse-adapted genotypes over time. We posit that intraspecific variation in Bb host breadth and specificity helps maintain overall species fitness in response to transmission by a generalist vector. Because pathogen genotypes vary in host breadth and result in diverse human disease manifestations, our findings indicate that a more nuanced definition of ‘host competence’ incorporating local genotype frequency is warranted.more » « less
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Reisen, William (Ed.)Abstract The incidence of tick-borne diseases has increased in recent decades and accounts for the majority of vector-borne disease cases in temperate areas of Europe, North America, and Asia. This emergence has been attributed to multiple and interactive drivers including changes in climate, land use, abundance of key hosts, and people’s behaviors affecting the probability of human exposure to infected ticks. In this forum paper, we focus on how land use changes have shaped the eco-epidemiology of Ixodes scapularis-borne pathogens, in particular the Lyme disease spirochete Borrelia burgdorferi sensu stricto in the eastern United States. We use this as a model system, addressing other tick-borne disease systems as needed to illustrate patterns or processes. We first examine how land use interacts with abiotic conditions (microclimate) and biotic factors (e.g., host community composition) to influence the enzootic hazard, measured as the density of host-seeking I. scapularis nymphs infected with B. burgdorferi s.s. We then review the evidence of how specific landscape configuration, in particular forest fragmentation, influences the enzootic hazard and disease risk across spatial scales and urbanization levels. We emphasize the need for a dynamic understanding of landscapes based on tick and pathogen host movement and habitat use in relation to human resource provisioning. We propose a coupled natural-human systems framework for tick-borne diseases that accounts for the multiple interactions, nonlinearities and feedbacks in the system and conclude with a call for standardization of methodology and terminology to help integrate studies conducted at multiple scales.more » « less
