Ecological Factors Affecting Infection Risk and Population Genetic Diversity of a Novel Potyvirus in Its Native Wild Ecosystem

Abstract

Increasing evidence indicates that there is ample diversity of plant virus species in wild ecosystems. The vast majority of this diversity, however, remains uncharacterized. Moreover, in these ecosystems the factors affecting plant virus infection risk and population genetic diversity, two traits intrinsically linked to virus emergence, are largely unknown. Along 3 years, we have analyzed the prevalence and diversity of plant virus species from the genus Potyvirus in evergreen oak forests of the Iberian Peninsula, the main wild ecosystem in this geographic region and in the entire Mediterranean basin. During this period, we have also measured plant species diversity, host density, plant biomass, temperature, relative humidity, and rainfall. Results indicated that potyviruses were always present in evergreen oak forests, with a novel virus species explaining the largest fraction of potyvirus-infected plants. We determined the genomic sequence of this novel virus and we explored its host range in natural and greenhouse conditions. Natural host range was limited to the perennial plant mountain rue (Ruta montana), commonly found in evergreen oak forests of the Iberian Peninsula. In this host, the virus was highly prevalent and was therefore provisionally named mediterranean ruda virus (MeRV). Focusing in this natural host–virus interaction, we analyzed the ecological factors affecting MeRV infection risk and population genetic diversity in its native wild ecosystem. The main predictor of virus infection risk was the host density. MeRV prevalence was the major factor determining genetic diversity and selection pressures in the virus populations. This observation supports theoretical predictions assigning these two traits a key role in parasite epidemiology and evolution. Thus, our analyses contribute both to characterize viral diversity and to understand the ecological determinants of virus population dynamics in wild ecosystems.

The Potyviruses: An Evolutionary Synthesis Is Emerging

“…The ω values for individual HarMV genes ( Figure 7) have a pattern within those of the other viruses, and with no evidence from Tajima's D tests of a major recent population expansion. The HarMV population was more variable than that of Mediterranean ruda potyvirus (MeRV), which has a similar ecology [87].…”

Ecological determinants of Potyvirus emergence in wild ecosystems

“…Besides the damage that potyviruses can cause in crops, some of them have been reported to infect weeds (e.g. dos Santos Martins et al, 2016;McLeish et al, 2017) and wild plant species (Malpica et al, 2006;, and symptoms induced by potyviruses in wild plant communities are not always obvious (Rodríguez-Nevado et al, 2017). Few studies have investigated potyvirus presence in wild ecosystems of the Iberian Peninsula, and such studies often focused in potyviruses known to be crop pathogens , but see Rodríguez-Nevado et al, 2017.…”

“…In addition, given that agricultural lands occupy more than a third of Spain territory, evergreen oak forests and other natural ecosystems are often adjacent to agroecosystems (see section 1.4), which favours plant virus dispersal between both types of ecosystems (Alexander et al, 2014). Thus, potyviruses present in wild ecosystems may have the potential to cause epidemics in adjacent crops Rodríguez-Nevado et al, 2017). Despite this ecological and economic relevance, the factors affecting potyvirus infection risk and population genetic structure in wild ecosystems remain largely unexplored.…”

“…However, recent studies have shown that plant viruses are widespread and highly diverse in wild ecosystems (Roossinck, 2012;Stobbe and Roossinck, 2014). Few studies however have investigated the genetic diversity of plant virus populations in wild ecosystems and their prevalence in native wild hosts (Malpica et al, 2006;Rodríguez-Nevado et al, 2017). In this thesis, the presence of species of the genus Potyvirus was investigated in evergreen oak and riparian forests of the Iberian Peninsula.…”

“…This is the largest genus of plant viruses and contains species that are major crop pathogens (e.g. Walsh and Jenner, 2002;Quenouille et al, 2013), together with species that have been reported to infect wild hosts (Malpica et al, 2006;Rodríguez-Nevado et al, 2017). This suggests that potyviruses may be important ecological agents in wild ecosystems (perhaps including evergreen oak and riparian forests), and with potential to cause epidemics in adjacent crops.…”