Landscape genetics reveals focal transmission of a human macroparasite.

Macroparasite infections (e.g., helminths) remain a major human health concern. However, assessing transmission dynamics is problematic because the direct observation of macroparasite dispersal among hosts is not possible. We used a novel landscape genetics approach to examine transmission of the hu...

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Main Authors: Charles D Criscione, Joel D Anderson, Dan Sudimack, Janardan Subedi, Ram P Upadhayay, Bharat Jha, Kimberly D Williams, Sarah Williams-Blangero, Timothy J C Anderson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-04-01
Series:PLoS Neglected Tropical Diseases
Online Access:http://europepmc.org/articles/PMC2857643?pdf=render
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spelling doaj-76e6b8768c1343a39fcf54a3abc624252020-11-24T21:58:51ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352010-04-0144e66510.1371/journal.pntd.0000665Landscape genetics reveals focal transmission of a human macroparasite.Charles D CriscioneJoel D AndersonDan SudimackJanardan SubediRam P UpadhayayBharat JhaKimberly D WilliamsSarah Williams-BlangeroTimothy J C AndersonMacroparasite infections (e.g., helminths) remain a major human health concern. However, assessing transmission dynamics is problematic because the direct observation of macroparasite dispersal among hosts is not possible. We used a novel landscape genetics approach to examine transmission of the human roundworm Ascaris lumbricoides in a small human population in Jiri, Nepal. Unexpectedly, we found significant genetic structuring of parasites, indicating the presence of multiple transmission foci within a small sampling area ( approximately 14 km(2)). We analyzed several epidemiological variables, and found that transmission is spatially autocorrelated around households and that transmission foci are stable over time despite extensive human movement. These results would not have been obtainable via a traditional epidemiological study based on worm counts alone. Our data refute the assumption that a single host population corresponds to a single parasite transmission unit, an assumption implicit in many classic models of macroparasite transmission. Newer models have shown that the metapopulation-like pattern observed in our data can adversely affect targeted control strategies aimed at community-wide impacts. Furthermore, the observed metapopulation structure and local mating patterns generate an excess of homozygotes that can accelerate the spread of recessive traits such as drug resistance. Our study illustrates how molecular analyses complement traditional epidemiological information in providing a better understanding of parasite transmission. Similar landscape genetic approaches in other macroparasite systems will be warranted if an accurate depiction of the transmission process is to be used to inform effective control strategies.http://europepmc.org/articles/PMC2857643?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Charles D Criscione
Joel D Anderson
Dan Sudimack
Janardan Subedi
Ram P Upadhayay
Bharat Jha
Kimberly D Williams
Sarah Williams-Blangero
Timothy J C Anderson
spellingShingle Charles D Criscione
Joel D Anderson
Dan Sudimack
Janardan Subedi
Ram P Upadhayay
Bharat Jha
Kimberly D Williams
Sarah Williams-Blangero
Timothy J C Anderson
Landscape genetics reveals focal transmission of a human macroparasite.
PLoS Neglected Tropical Diseases
author_facet Charles D Criscione
Joel D Anderson
Dan Sudimack
Janardan Subedi
Ram P Upadhayay
Bharat Jha
Kimberly D Williams
Sarah Williams-Blangero
Timothy J C Anderson
author_sort Charles D Criscione
title Landscape genetics reveals focal transmission of a human macroparasite.
title_short Landscape genetics reveals focal transmission of a human macroparasite.
title_full Landscape genetics reveals focal transmission of a human macroparasite.
title_fullStr Landscape genetics reveals focal transmission of a human macroparasite.
title_full_unstemmed Landscape genetics reveals focal transmission of a human macroparasite.
title_sort landscape genetics reveals focal transmission of a human macroparasite.
publisher Public Library of Science (PLoS)
series PLoS Neglected Tropical Diseases
issn 1935-2727
1935-2735
publishDate 2010-04-01
description Macroparasite infections (e.g., helminths) remain a major human health concern. However, assessing transmission dynamics is problematic because the direct observation of macroparasite dispersal among hosts is not possible. We used a novel landscape genetics approach to examine transmission of the human roundworm Ascaris lumbricoides in a small human population in Jiri, Nepal. Unexpectedly, we found significant genetic structuring of parasites, indicating the presence of multiple transmission foci within a small sampling area ( approximately 14 km(2)). We analyzed several epidemiological variables, and found that transmission is spatially autocorrelated around households and that transmission foci are stable over time despite extensive human movement. These results would not have been obtainable via a traditional epidemiological study based on worm counts alone. Our data refute the assumption that a single host population corresponds to a single parasite transmission unit, an assumption implicit in many classic models of macroparasite transmission. Newer models have shown that the metapopulation-like pattern observed in our data can adversely affect targeted control strategies aimed at community-wide impacts. Furthermore, the observed metapopulation structure and local mating patterns generate an excess of homozygotes that can accelerate the spread of recessive traits such as drug resistance. Our study illustrates how molecular analyses complement traditional epidemiological information in providing a better understanding of parasite transmission. Similar landscape genetic approaches in other macroparasite systems will be warranted if an accurate depiction of the transmission process is to be used to inform effective control strategies.
url http://europepmc.org/articles/PMC2857643?pdf=render
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