Characteristics and drivers of plant virus community spatial patterns in US west coast grasslands

Abstract

The spatial distribution of disease risk caused by multi‐pathogen infections is not frequently characterized, limiting understanding of the drivers of infection and thwarting prediction of future risk in a changing environment. Further complicating this predictive understanding is that interactions among multiple pathogens within a host commonly alter transmission success, infection risk, and disease dynamics. By characterizing spatial patterns of Barley and Cereal Yellow Dwarf Virus (B/CYDV) infections that range from the scale of an individual plant to thousands of neighboring plants, we examined the contributions of spatial processes to the distribution of disease risk. In a two‐year field experiment, we planted grass hosts of B/CYDVs into fertilized plots of US west coast grasslands. We determined how vector‐sharing, environmental conditions and spatial variation in host quality affected spatial patterns of single viruses, pairs of viruses and the whole virus community across out‐planted grass hosts. We found that single viruses and virus communities were spatially random, indicating that infection does not solely spread through the community in a wave‐like manner. On the other hand, we found that pairs of viruses, especially those that share a vector species, were aggregated spatially. This suggests that if within‐host competition exists, it is not strong. Aggregation in one pair of viruses was more frequent due to environmental conditions and spatial variation in out‐planted host quality, measured as vector preference. These results highlight the importance of insect vectors for predicting the spatial distribution of coinfection risk by B/CYDVs.

Mixed infection, risk projection, and misdirection: Interactions among pathogens alter links between host resources and disease

“…Moreover, infection risk is not determined exclusively by dynamics operating within hosts: It also depends on exposure to pathogens. For vector‐borne pathogens, inherent differences in vector ecology therefore play a large role in determining risk of infection by different pathogens (Kendig et al., 2017; Seabloom et al., 2013; Strauss et al., 2020). From a theoretical perspective, R* theory can be nested within a metacommunity framework—where each patch is a host—to link resource ratios to disease dynamics both within and among hosts (Borer et al., 2016; Strauss et al., 2019).…”

“…Hereafter, we refer to these viruses as SGV, PAV, and RPV, respectively. Coinfections among two or more viruses are common in natural plant communities (Seabloom et al., 2010) and agricultural settings (Rochow, 1979), especially for viruses that share vectors (Kendig et al., 2017). In a field study that tested for presence of five B/CYDVs (including SGV, PAV, and RPV), mean viral richness in infected hosts ranged from ~2–3 unique virus species (Seabloom et al., 2013).…”

“…B/CYDVs are well suited to study relationships between resource availability and infection risk, because they respond to variation in nitrogen and phosphorus supply to hosts (Rua et al, 2013;Seabloom et al, 2009). Some of the observed virus responses in the field (Kendig et al, 2017;Seabloom et al, 2010Seabloom et al, , 2013) could reflect effects of nutrients on aphid demography or behavior (Strauss et al, 2020). In contrast, responses in laboratory experiments with controlled aphid exposure can isolate effects of the resource environment of the host (i.e., tissue chemistry).…”

“…Here, we experimentally ask whether exposure to multiple pathogens alters relationships between resources and disease risk using a naturally co‐occurring community of plant viruses. We hypothesized that rates of infection by three viruses in isolation would differ with nitrogen (N) or phosphorus (P) supply and that the strength of interactions among the viruses would also vary with host resources, as suggested by laboratory experiments (Kendig et al., 2020; Lacroix et al., 2014), field experiments (Kendig et al., 2017; Seabloom et al., 2013), and field observations (Seabloom et al., 2010). We grew grass hosts ( Avena sativa ) under crossed gradients of N and P (three levels each) and exposed them to three species of barley and cereal yellow dwarf virus (CYDV‐RPV, BYDV‐SGV, and BYDV‐PAV), either singly or jointly.…”

The Epidemiology of Plant Virus Disease: Towards a New Synthesis

“…In field studies of barley and cereal yellow dwarf viruses in US west coast grasslands, the effect of shared vectors, environmental conditions and spatial variation in hosts affected the spatial variation of single viruses, paired viruses and the whole virus community in grass hosts [ 242 ]. It was found that for single viruses and the whole virus community, there was a random spatial distribution which was considered to reflect a random pattern of spread.…”