Dataset Information

A multi-scale analysis of influenza A virus fitness trade-offs due to temperature-dependent virus persistence.

ABSTRACT: Successful replication within an infected host and successful transmission between hosts are key to the continued spread of most pathogens. Competing selection pressures exerted at these different scales can lead to evolutionary trade-offs between the determinants of fitness within and between hosts. Here, we examine such a trade-off in the context of influenza A viruses and the differential pressures exerted by temperature-dependent virus persistence. For a panel of avian influenza A virus strains, we find evidence for a trade-off between the persistence at high versus low temperatures. Combining a within-host model of influenza infection dynamics with a between-host transmission model, we study how such a trade-off affects virus fitness on the host population level. We show that conclusions regarding overall fitness are affected by the type of link assumed between the within- and between-host levels and the main route of transmission (direct or environmental). The relative importance of virulence and immune response mediated virus clearance are also found to influence the fitness impacts of virus persistence at low versus high temperatures. Based on our results, we predict that if transmission occurs mainly directly and scales linearly with virus load, and virulence or immune responses are negligible, the evolutionary pressure for influenza viruses to evolve toward good persistence at high within-host temperatures dominates. For all other scenarios, influenza viruses with good environmental persistence at low temperatures seem to be favored.

SUBMITTER: Handel A

PROVIDER: S-EPMC3605121 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

A multi-scale analysis of influenza A virus fitness trade-offs due to temperature-dependent virus persistence.

Handel Andreas A Brown Justin J Stallknecht David D Rohani Pejman P

PLoS computational biology 20130321 3

Successful replication within an infected host and successful transmission between hosts are key to the continued spread of most pathogens. Competing selection pressures exerted at these different scales can lead to evolutionary trade-offs between the determinants of fitness within and between hosts. Here, we examine such a trade-off in the context of influenza A viruses and the differential pressures exerted by temperature-dependent virus persistence. For a panel of avian influenza A virus stra ...[more]

PMID: 23555223

Similar Datasets

Project description:The acquisition of new hosts provides a virus with more opportunities for transmission and survival but may be limited by across-host fitness trade-offs. Major causes of across-host trade-offs are antagonistic pleiotropy, that is, host differential phenotypic effects of mutations, a Genotype x Environment interaction, and epistasis, a Genotype x Genotype interaction. Here, we analyze if there are trade-offs, and what are the causes, associated with the acquisition by tobacco mild green mosaic virus (TMGMV) of a new host. For this, the multiplication of sympatric field isolates of TMGMV from its wild reservoir host Nicotiana glauca and from pepper crops was quantified in the original and the heterologous hosts. TMGMV isolates from N. glauca were adapted to their host, but pepper isolates were not adapted to pepper, and the acquisition of this new host was associated with a fitness penalty in the original host. Analyses of the collection of field isolates and of mutant genotypes derived from biologically active cDNA clones showed a role of mutations in the coat protein and the 3' untranslated region in determining within-host virus fitness. Fitness depended on host-specific effects of these mutations, on the genetic background in which they occurred, and on higher-order interactions of the type Genotype x Genotype x Environment. These types of effects had been reported to generate across-host fitness trade-offs under experimental evolution. Our results show they may also operate in heterogeneous natural environments and could explain why pepper isolates were not adapted to pepper and their lower fitness in N. glauca IMPORTANCE The acquisition of new hosts conditions virus epidemiology and emergence; hence it is important to understand the mechanisms behind host range expansion. Experimental evolution studies have identified antagonistic pleiotropy and epistasis as genetic mechanisms that limit host range expansion, but studies from virus field populations are few. Here, we compare the performance of isolates of tobacco mild green mosaic virus from its reservoir host, Nicotiana glauca, and its new host, pepper, showing that acquisition of a new host was not followed by adaptation to it but was associated with a fitness loss in the original host. Analysis of mutations determining host-specific virus multiplication identified antagonistic pleiotropy, epistasis, and host-specific epistasis as mechanisms generating across-host fitness trade-offs that may prevent adaptation to pepper and cause a loss of fitness in N. glauca Thus, mechanisms determining trade-offs, identified under experimental evolution, could also operate in the heterogeneous environment in which natural plant virus populations occur.

Project description:Theoretically, homogeneous environments favor the evolution of specialists whereas heterogeneous environments favor generalists. Canine distemper is a multi-host carnivore disease caused by canine distemper virus (CDV). The described cell receptor of CDV is SLAM (CD150). Attachment of CDV hemagglutinin protein (CDV-H) to this receptor facilitates fusion and virus entry in cooperation with the fusion protein (CDV-F). We investigated whether CDV strains co-evolved in the large, homogeneous domestic dog population exhibited specialist traits, and strains adapted to the heterogeneous environment of smaller populations of different carnivores exhibited generalist traits. Comparison of amino acid sequences of the SLAM binding region revealed higher similarity between sequences from Canidae species than to sequences from other carnivore families. Using an in vitro assay, we quantified syncytia formation mediated by CDV-H proteins from dog and non-dog CDV strains in cells expressing dog, lion or cat SLAM. CDV-H proteins from dog strains produced significantly higher values with cells expressing dog SLAM than with cells expressing lion or cat SLAM. CDV-H proteins from strains of non-dog species produced similar values in all three cell types, but lower values in cells expressing dog SLAM than the values obtained for CDV-H proteins from dog strains. By experimentally changing one amino acid (Y549H) in the CDV-H protein of one dog strain we decreased expression of specialist traits and increased expression of generalist traits, thereby confirming its functional importance. A virus titer assay demonstrated that dog strains produced higher titers in cells expressing dog SLAM than cells expressing SLAM of non-dog hosts, which suggested possible fitness benefits of specialization post-cell entry. We provide in vitro evidence for the expression of specialist and generalist traits by CDV strains, and fitness trade-offs across carnivore host environments caused by antagonistic pleiotropy. These findings extend knowledge on CDV molecular epidemiology of particular relevance to wild carnivores.

Dataset Information

A multi-scale analysis of influenza A virus fitness trade-offs due to temperature-dependent virus persistence.

Publications

A multi-scale analysis of influenza A virus fitness trade-offs due to temperature-dependent virus persistence.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets