The scale-of-choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

Predicting viral emergence is difficult due to the stochastic nature of the underlying processes and the many factors that govern pathogen evolution. Environmental factors affecting the host, the pathogen and the interaction between both are key in emergence. In particular, infectious disease dynamics are affected by spatiotemporal heterogeneity in their environments. A broad knowledge of these factors will allow better estimating where and when viral emergence is more likely to occur. Here, we investigate how the population structure for susceptibility-to-infection genes of the plant Arabidopsis thaliana shapes the evolution of Turnip mosaic virus (TuMV). For doing so we have evolved TuMV lineages in two radically different host population structures: (1) a metapopulation subdivided into six demes (subpopulations); each one being composed of individuals from only one of six possible A. thaliana ecotypes and (2) a well-mixed population constituted by equal number of plants from the same six A. thaliana ecotypes. These two populations were evolved for twelve serial passages. At the end of the experimental evolution, we found faster adaptation of TuMV to each ecotype in the metapopulation than in the well-mixed heterogeneous host populations. However, viruses evolved in well-mixed populations were more pathogenic and infectious than viruses evolved in the metapopulation. Furthermore, the viruses evolved in the demes showed stronger signatures of local specialization than viruses evolved in the well-mixed populations. These results illustrate how the genetic diversity of hosts in an experimental ecosystem favors the evolution of virulence of a pathogen.

Environmental conditions are an important factor driving pathogens’ evolution. Here, we explore the effects of drought stress in plant virus evolution. We evolved turnip mosaic potyvirus in well-watered and drought conditions in Arabidopsis thaliana accessions that differ in their response to virus infection. Virus adaptation occurred in all accessions independently of watering status. Drought-evolved viruses conferred a significantly higher drought tolerance to infected plants. By contrast, nonsignificant increases in tolerance were observed in plants infected with viruses evolved under standard watering. The magnitude of this effect was dependent on the plant accessions. Differences in tolerance were correlated to alterations in the expression of host genes, some involved in regulation of the circadian clock, as well as in deep changes in the balance of phytohormones regulating defense and growth signaling pathways. Our results show that viruses can promote host survival in situations of abiotic stress, with the magnitude of such benefit being a selectable trait.