Host Abundance and Identity Determine the Epidemiology and Evolution of a Generalist Plant Virus in a Wild Ecosystem

Abstract

Increasing evidence indicates that in wild ecosystems plant viruses are important ecological agents, and with potential to jump into crops, but only recently have the diversity and population dynamics of wild plant viruses begun to be explored. Theory proposes that biotic factors (e.g., ecosystem biodiversity, host abundance, and host density) and climatic conditions would determine the epidemiology and evolution of wild plant viruses. However, these predictions seldom have been empirically tested. For 3 years, we analyzed the prevalence and genetic diversity of Potyvirus species in preserved riparian forests of Spain. Results indicated that potyviruses were always present in riparian forests, with a novel generalist potyvirus species provisionally named Iberian hop mosaic virus (IbHMV), explaining the largest fraction of infected plants. Focusing on this potyvirus, we analyzed the biotic and climatic factors affecting virus infection risk and population genetic diversity in its native ecosystem. The main predictors of IbHMV infection risk were host relative abundance and species richness. Virus prevalence and host relative abundance were the major factors determining the genetic diversity and selection pressures in the virus population. These observations support theoretical predictions assigning these ecological factors a key role in parasite epidemiology and evolution. Finally, our phylogenetic analysis indicated that the viral population was genetically structured according to host and location of origin, as expected if speciation is largely sympatric. Thus, this work contributes to characterizing viral diversity and provides novel information on the determinants of plant virus epidemiology and evolution in wild ecosystems.

Determinants of Virus Variation, Evolution, and Host Adaptation

“…Environmental conditions directly impact virus infection, prevalence, evolution, and host interactions. These include abiotic factors like temperature, water stress, CO 2 levels, ecology, community makeup, and population heterogeneity [5,26,74,75]. Viruses, hosts, and vectors exist within a given ecosystem, which can impact the spread, disease risk, and symptoms of virus infections.…”

“…Accordingly, virus evolution is also impacted by ecological factors such as host abundance and species richness, which are affected by climate change and land use [74,76]. In some cases, a loss of biodiversity in host communities is correlated with increased disease [75]. However, adding genetic diversity can amplify disease incidence if hosts are susceptible or host density increases [77].…”

The impact of climate change on disease in wild plant populations and communities

“…Other research has been aimed at specific ecosystems in which a range of hosts are affected by one or more pathogens and where climate change has been shown, or is proposed, as an important factor in plant community structure (Table 3). The research topics carried out at the ecosystem level is again disparate: P. cinnamomi and P. cambivora affecting endemic flora (Barrett & Yates, 2015;Hill et al, 2009;Rigg et al, 2018), fire, climate change, and myrtle rust Fernandez Winzer et al, 2020), subantarctic habitats and soilborne diseases (Whinam et al, 2014), Iberian hop mosaic virus in a wild ecosystem (Rodrígues-Nevado et al, 2020), and species distribution models for an endemic marsupial based in part on tree and shrub diebacks (Molloy et al, 2016).…”

Alteration of plant species mixtures by virus infection: Managed pastures the forgotten dimension

“…They also include plants growing in disturbed or undisturbed natural vegetation, and at the interface between managed and natural vegetation (Alexander et al, 2014, 2017; Bernardo et al, 2018; Bos, 1981; Cooper & Jones, 2006; Ingwell & Bosque‐Pérez, 2015; Ingwell et al, 2017; Jones, 2009; Jones & Coutts, 2015; Malmstrom & Alexander, 2016; Malmstrom et al, 2011, 2017; Prendeville et al, 2012; Roossinck, 2013; Thresh, 1981; Vincent et al, 2014; Webster et al, 2007). The viruses present may be generalists with broad host ranges or specialists with narrow host ranges (Borer et al, 2010; Cooper & Jones, 2006; Jones, 2009; Rodríguez‐Nevado et al, 2020; Thresh, 1980, 1981). The question then arises concerning the extent by which virus infection occurring in one or more plant species within a mixture can alter the species balance by influencing an infected species’ ability to compete with intermingling or nearby plants belonging to the other species.…”