title: Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses.
abstract: Trade-offs between different components of a pathogen's replication and transmission cycle are thought to be common. A number of studies have identified trade-offs that emerge across scales, reflecting the tension between strategies that optimize within-host proliferation and large-scale population spread. Most of these studies are theoretical in nature, with direct experimental tests of such cross-scale trade-offs still rare. Here, we report an analysis of avian influenza A viruses across scales, focusing on the phenotype of temperature-dependent viral persistence. Taking advantage of a unique dataset that reports both environmental virus decay rates and strain-specific viral kinetics from duck challenge experiments, we show that the temperature-dependent environmental decay rate of a strain does not impact within-host virus load. Hence, for this phenotype, the scales of within-host infection dynamics and between-host environmental persistence do not seem to interact: viral fitness may be optimized on each scale without cross-scale trade-offs. Instead, we confirm the existence of a temperature-dependent persistence trade-off on a single scale, with some strains favouring environmental persistence in water at low temperatures while others reduce sensitivity to increasing temperatures. We show that this temperature-dependent trade-off is a robust phenomenon and does not depend on the details of data analysis. Our findings suggest that viruses might employ different environmental persistence strategies, which facilitates the coexistence of diverse strains in ecological niches. We conclude that a better understanding of the transmission and evolutionary dynamics of influenza A viruses probably requires empirical information regarding both within-host dynamics and environmental traits, integrated within a combined ecological and within-host framework.
authors.affiliation: Department of Epidemiology and Biostatistics, College of Public Health, The University of Georgia, Athens, GA 30602, USA ahandel@uga.edu.
authors.forename: Andreas
authors.initials: A
authors.lastname: Handel
authors.affiliation: University of Reunion Island, Avenue René Cassin, Saint-Denis Cedex 97715, Reunion Island.
authors.forename: Camille
authors.initials: C
authors.lastname: Lebarbenchon
authors.affiliation: Department of Population Health, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602, USA.
authors.forename: David
authors.initials: D
authors.lastname: Stallknecht
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Center for the Study of Complex Systems, University of Michigan, Ann Arbor, MI 48109, USA Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA.
authors.forename: Pejman
authors.initials: P
authors.lastname: Rohani
mesh_terms: D000818:Animals; D005075:Biological Evolution; D001715:Bird Diseases / Q000635:transmission / Q000821:virology*; D004372:Ducks; D005618:Fresh Water / Q000821:virology; D056084:Genetic Fitness; D006801:Humans; D009980:Influenza A virus / Q000235:genetics / Q000502:physiology*; D005585:Influenza in Birds / Q000635:transmission / Q000821:virology*; D007251:Influenza, Human / Q000635:transmission / Q000821:virology; D008910:Minnesota; D008954:Models, Biological; D010641:Phenotype; D013696:Temperature; D019562:Viral Load / Q000662:veterinary*
keywords: avian influenza; environmental persistence; mathematical model; multi-scale analysis