Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections

<p>Abstract</p> <p>Background</p> <p>Evolutionary theory suggests that the selection pressure on parasites to maximize their transmission determines their optimal host exploitation strategies and thus their virulence. Establishing the adaptive basis to parasite life his...

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Main Authors: Nithiuthai S, Müller-Graf CDM, Lafond T, Paul REL, Brey PT, Koella JC
Format: Article
Language:English
Published: BMC 2004-09-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/4/30
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author Nithiuthai S
Müller-Graf CDM
Lafond T
Paul REL
Brey PT
Koella JC
author_facet Nithiuthai S
Müller-Graf CDM
Lafond T
Paul REL
Brey PT
Koella JC
author_sort Nithiuthai S
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Evolutionary theory suggests that the selection pressure on parasites to maximize their transmission determines their optimal host exploitation strategies and thus their virulence. Establishing the adaptive basis to parasite life history traits has important consequences for predicting parasite responses to public health interventions. In this study we examine the extent to which malaria parasites conform to the predicted adaptive trade-off between transmission and virulence, as defined by mortality. The majority of natural infections, however, result in sub-lethal virulent effects (e.g. anaemia) and are often composed of many strains. Both sub-lethal effects and pathogen population structure have been theoretically shown to have important consequences for virulence evolution. Thus, we additionally examine the relationship between anaemia and transmission in single and mixed clone infections.</p> <p>Results</p> <p>Whereas there was a trade-off between transmission success and virulence as defined by host mortality, contradictory clone-specific patterns occurred when defining virulence by anaemia. A negative relationship between anaemia and transmission success was found for one of the parasite clones, whereas there was no relationship for the other. Notably the two parasite clones also differed in a transmission phenotype (gametocyte sex ratio) that has previously been shown to respond adaptively to a changing blood environment. In addition, as predicted by evolutionary theory, mixed infections resulted in increased anaemia. The increased anaemia was, however, not correlated with any discernable parasite trait (e.g. parasite density) or with increased transmission.</p> <p>Conclusions</p> <p>We found some evidence supporting the hypothesis that there is an adaptive basis correlating virulence (as defined by host mortality) and transmission success in malaria parasites. This confirms the validity of applying evolutionary virulence theory to biomedical research and adds support to the prediction that partially effective vaccines may select for increasingly virulent malaria parasite strains. By contrast, there was no consistent correlation between transmission and sub-lethal anaemia, a more common outcome of malaria infection. However, overall, the data are not inconsistent with the recent proposal that sub-lethal effects may impose an upper limit on virulence. Moreover, clone specific differences in transmission phenotypes linked to anaemia do suggest that there is considerable adaptive potential relating anaemia and transmission that may lead to uncertain consequences following intervention strategies.</p>
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spelling doaj.art-22447d106987424e9ef49ab1f4b286632022-12-21T23:12:31ZengBMCBMC Evolutionary Biology1471-21482004-09-01413010.1186/1471-2148-4-30Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infectionsNithiuthai SMüller-Graf CDMLafond TPaul RELBrey PTKoella JC<p>Abstract</p> <p>Background</p> <p>Evolutionary theory suggests that the selection pressure on parasites to maximize their transmission determines their optimal host exploitation strategies and thus their virulence. Establishing the adaptive basis to parasite life history traits has important consequences for predicting parasite responses to public health interventions. In this study we examine the extent to which malaria parasites conform to the predicted adaptive trade-off between transmission and virulence, as defined by mortality. The majority of natural infections, however, result in sub-lethal virulent effects (e.g. anaemia) and are often composed of many strains. Both sub-lethal effects and pathogen population structure have been theoretically shown to have important consequences for virulence evolution. Thus, we additionally examine the relationship between anaemia and transmission in single and mixed clone infections.</p> <p>Results</p> <p>Whereas there was a trade-off between transmission success and virulence as defined by host mortality, contradictory clone-specific patterns occurred when defining virulence by anaemia. A negative relationship between anaemia and transmission success was found for one of the parasite clones, whereas there was no relationship for the other. Notably the two parasite clones also differed in a transmission phenotype (gametocyte sex ratio) that has previously been shown to respond adaptively to a changing blood environment. In addition, as predicted by evolutionary theory, mixed infections resulted in increased anaemia. The increased anaemia was, however, not correlated with any discernable parasite trait (e.g. parasite density) or with increased transmission.</p> <p>Conclusions</p> <p>We found some evidence supporting the hypothesis that there is an adaptive basis correlating virulence (as defined by host mortality) and transmission success in malaria parasites. This confirms the validity of applying evolutionary virulence theory to biomedical research and adds support to the prediction that partially effective vaccines may select for increasingly virulent malaria parasite strains. By contrast, there was no consistent correlation between transmission and sub-lethal anaemia, a more common outcome of malaria infection. However, overall, the data are not inconsistent with the recent proposal that sub-lethal effects may impose an upper limit on virulence. Moreover, clone specific differences in transmission phenotypes linked to anaemia do suggest that there is considerable adaptive potential relating anaemia and transmission that may lead to uncertain consequences following intervention strategies.</p>http://www.biomedcentral.com/1471-2148/4/30
spellingShingle Nithiuthai S
Müller-Graf CDM
Lafond T
Paul REL
Brey PT
Koella JC
Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
BMC Evolutionary Biology
title Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
title_full Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
title_fullStr Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
title_full_unstemmed Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
title_short Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections
title_sort experimental evaluation of the relationship between lethal or non lethal virulence and transmission success in malaria parasite infections
url http://www.biomedcentral.com/1471-2148/4/30
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