Restriction of Francisella novicida genetic diversity during infection of the vector midgut.

The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circula...

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Main Authors: Kathryn E Reif, Guy H Palmer, David W Crowder, Massaro W Ueti, Susan M Noh
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-10-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC4231110?pdf=render
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spelling doaj-3f2f8d6c6d8543b7a2dffddd3f8e38842020-11-25T01:47:09ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742014-10-011010e100449910.1371/journal.ppat.1004499Restriction of Francisella novicida genetic diversity during infection of the vector midgut.Kathryn E ReifGuy H PalmerDavid W CrowderMassaro W UetiSusan M NohThe genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.http://europepmc.org/articles/PMC4231110?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Kathryn E Reif
Guy H Palmer
David W Crowder
Massaro W Ueti
Susan M Noh
spellingShingle Kathryn E Reif
Guy H Palmer
David W Crowder
Massaro W Ueti
Susan M Noh
Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
PLoS Pathogens
author_facet Kathryn E Reif
Guy H Palmer
David W Crowder
Massaro W Ueti
Susan M Noh
author_sort Kathryn E Reif
title Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
title_short Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
title_full Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
title_fullStr Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
title_full_unstemmed Restriction of Francisella novicida genetic diversity during infection of the vector midgut.
title_sort restriction of francisella novicida genetic diversity during infection of the vector midgut.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2014-10-01
description The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.
url http://europepmc.org/articles/PMC4231110?pdf=render
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