Trends in Microbiology

Trends in Microbiology

Volume 11, Issue 9, September 2003, Pages 415-421
Journal home page for Trends in Microbiology

Questions on viral population biology to complete dengue puzzle

https://doi.org/10.1016/S0966-842X(03)00206-3Get rights and content

Abstract

The mechanisms driving the current evolution of dengue remain unclear. We argue that disregarding the population biology of viruses has been a limiting factor, and present a hypothetical framework based on viral population biology. This allows us to pinpoint three flaws that need to be addressed: (1) a large underestimation of the viral polymorphism within populations; (2) a disregard of viral loci other than that encoding the antigenic envelope; and (3) the neglect of host-driven selection, especially that of vector-driven selection.

Section snippets

Problems related to dengue morbidity and epidemics

Whatever the species involved, dengue disease displays various pathologies 13, 14, regrouped into three categories, ranking from silent infections to dengue fevers (DF) and dengue haemorrhagic fevers (DHF). This ranking order reflects both a gradual increase in morbidity and a gradual decrease in frequency. Indeed, silent infections are detected a posteriori through the immunization pattern, whereas hospitalization is often required for DF cases and is obligatory for DHF cases. Silent

Viral evolution within populations

A succession of evolutionary factors acts on viral polymorphism (Box 1). RNA viruses are characterized by the highest mutation rates known (∼10−4 per site and replication round), quick replication and large populations. All of these characteristics ensure the creation and maintenance of high genetic diversity within hosts [23]. Frequent recombination among viruses of the same DEN species 24, 25, 26 further enhances within-host diversity. Indeed, prediction of a high genetic diversity within the

Distribution of viral polymorphism among populations

The high levels of mutation, recombination and drift experienced within populations lead to the expectation of immigrating viruses rapidly diverging from their ancestral population. Any viral locus can thus be expected to display a large genetic differentiation among populations within DEN species. Rapid in situ evolution of viral polymorphism was indeed observed whenever investigators looked for it [25]. In addition, despite a large underestimation as a result of single-gene studies and sample

Host-driven selection

In vitro experiments suggest both the occurrence of host-driven selection and an antagonism between human- and vector-driven selection. It is well known that multiple passage in mosquitoes or in C6/36 mosquito cells attenuates the virulence of dengue viruses for mammalian cell cultures and vice versa [41]. However, very little is known about the targets of host-driven selection in the viral genome.

Direct investigation of the occurrence of host-driven selection was only undertaken for 3′NCR,

Conclusion

Initially, the implicit assumptions about dengue characteristics were that they would obey universal rules, in which case transmission would be controlled by vectors, whereas pathogenesis and morbidity would be co-regulated by human history and viral genetics. We suggest that this hypothetical framework is likely to be invalid (see also Refs [6] and [20] for complementary arguments). We also suggest that an alternative hypothetical framework, based on viral population biology, looks promising.

Acknowledgements

We are grateful to Thierry de Meeûs for his constant encouragement and helpful discussions. We also thank L. Rosen, F. Rodhain and M. Vazeille-Falcoz for interesting feedback on earlier drafts, as well as the Editor and referees for useful criticism and editing comments.

Glossary

Glossary

adaptation, co-adaptation, local adaptation/maladaptation:
qualify the results of selection in terms of fitness increase. Co-adaptation and local adaptation are specific to host-pathogen systems where each species imposes selection on the other. Local adaptation of pathogens denotes that they have better fitness when infecting local rather than foreign hosts (local adaptation of hosts results in better host resistance to infection by local, rather than foreign, pathogens). Opposite patterns

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