Abstract
Virulence determines the impact a pathogen has on the fitness of its host, yet current understanding of the evolutionary origins and causes of virulence of many pathogens is surprisingly incomplete. Here, we explore the evolution of Marek's disease virus (MDV), a herpesvirus commonly afflicting chickens and rarely other avian species. The history of MDV in the 20th century represents an important case study in the evolution of virulence. The severity of MDV infection in chickens has been rising steadily since the adoption of intensive farming techniques and vaccination programs in the 1950s and 1970s, respectively. It has remained uncertain, however, which of these factors is causally more responsible for the observed increase in virulence of circulating viruses. We conducted a phylogenomic study to understand the evolution of MDV in the context of dramatic changes to poultry farming and disease control. Our analysis reveals evidence of geographical structuring of MDV strains, with reconstructions supporting the emergence of virulent viruses independently in North America and Eurasia. Of note, the emergence of virulent viruses appears to coincide approximately with the introduction of comprehensive vaccination on both continents. The time‐dated phylogeny also indicated that MDV has a mean evolutionary rate of ~1.6 × 10−5 substitutions per site per year. An examination of gene‐linked mutations did not identify a strong association between mutational variation and virulence phenotypes, indicating that MDV may evolve readily and rapidly under strong selective pressures and that multiple genotypic pathways may underlie virulence adaptation in MDV.
Highlights
Understanding the evolution of virulence is a major focus of pathogen research and has important ramifications for evolutionary theory, host–parasite ecology, and epidemiology (Alizon, Hurford, Mideo, & Van Baalen, 2009; Cressler, McLeod, Rozins, van den Hoogen, & Day, 2016; Ebert, 1998; Schmid-Hempel, 2008, 2009, 2011; Woolhouse, Taylor, & Haydon, 2001)
Despite the importance of virulence evolution, the prevailing theory, which is based on a life-history trade-off framework (Anderson & May, 1982; Ewald, 1983), has to some extent suffered from a lack of empirical validation (Cressler et al, 2016)
Many of these factors seem counterintuitive from the perspective of disease prevention, but they indicate how substantially shortened host cohort durations, which have halved for broiler chickens in 60 years due to advances in nutrition and breeding (Anthony, 1998), could have inadvertently contributed to the evolution of increased virulence
Summary
Understanding the evolution of virulence is a major focus of pathogen research and has important ramifications for evolutionary theory, host–parasite ecology, and epidemiology (Alizon, Hurford, Mideo, & Van Baalen, 2009; Cressler, McLeod, Rozins, van den Hoogen, & Day, 2016; Ebert, 1998; Schmid-Hempel, 2008, 2009, 2011; Woolhouse, Taylor, & Haydon, 2001). Denser flocks and longer durations for rearing in combination with shorter intercohort intervals and limited virus elimination by cleaning and disinfection can lead to reduced MDV virulence Many of these factors seem counterintuitive from the perspective of disease prevention, but they indicate how substantially shortened host cohort durations, which have halved for broiler chickens in 60 years due to advances in nutrition and breeding (Anthony, 1998), could have inadvertently contributed to the evolution of increased virulence. Both vaccine use and intensive farming can influence pathogen transmission dramatically because they artificially manipulate the immune status and population dynamics of the host. We present findings from a phylogenomic study aimed at resolving the geographical, temporal, and ancestral trait patterns of MDV virulence evolution in the context of these changes
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