Phylogenetic structure and host abundance drive disease pressure in communities

Abstract

Pathogens play an important part in shaping the structure and dynamics of natural communities, because species are not affected by them equally 1,2 . A shared goal of ecology and epidemiology is to predict when a species is most vulnerable to disease. A leading hypothesis asserts that the impact of disease should increase with host abundance, producing a 'rare-species advantage' 3-5 . However, the impact of a pathogen may be decoupled from host abundance, because most pathogens infect more than one species, leading to pathogen spillover onto closely related species 6,7 . Here we show that the phylogenetic and ecological structure of the surrounding community can be important predictors of disease pressure. We found that the amount of tissue lost to disease increased with the relative abundance of a species across a grassland plant community, and that this rare-species advantage had an additional phylogenetic component: disease pressure was stronger on species with many close relatives. We used a global model of pathogen sharing as a function of relatedness between hosts, which provided a robust predictor of relative disease pressure at the local scale. In our grassland, the total amount of disease was most accurately explained not by the abundance of the focal host alone, but by the abundance of all species in the community weighted by their phylogenetic distance to the host. Furthermore, the model strongly predicted observed disease pressure for 44 novel host species we introduced experimentally to our study site, providing evidence for a mechanism to explain why phylogenetically rare species are more likely to become invasive when introduced 8,9 . Our results demonstrate how the phylogenetic and ecological structure of communities can have a key role in disease dynamics, with implications for the maintenance of biodiversity, biotic resistance against introduced weeds, and the success of managed plants in agriculture and forestry.Plant pathogens can be important drivers of community diversity, structure and dynamics 1,2,10,11 . A basic premise of epidemiology is that pathogen transmission often increases with host density 12,13 . Densitydependent disease provides a mechanism for the maintenance of plant diversity in natural communities, in which locally uncommon species enjoy a rare-species advantage-based on lower enemy pressure-that mitigates the competitive impacts of dominant species 3-5 . Reports of density-dependent disease dynamics generally infer the potential effects on communities from studies of one or a few species 2 , while community-level studies 1 are scarce but essential to evaluate whether such a rarespecies advantage predicts patterns of disease across a community.An ongoing debate concerns how community context influences disease, and particularly whether biodiversity suppresses infection and emerging diseases 14,15 . If increasing the number of species in a community reduces the density of competent hosts or the frequency of infected vectors, then biodiversity shows a suppressive 'dilution e...

The strength of negative plant–soil feedback increases from the intraspecific to the interspecific and the functional group level

“…Closely related species may still accumulate distinct soil communities leading to differences in plant performance when growing in different soil types and therefore to different feedback effects (Pendergast, Burke, & Carson, 2013). In contrast to that, other studies have shown that more closely related plant species may be more similar to each other than to distinctly related species with regard to the composition of specific soil communities (Gilbert & Webb, 2007; Webb et al., 2006) as well as in terms of ecological traits such as germination rate, seedling survival (Burns & Strauss, 2011), and responses to infestation by pathogens (Gilbert et al., 2015; Parker et al., 2015). Contrary to our expectations, we did not find such a relationship between feedback strength and species‐specific morphological or functional traits of the involved accessions/species.…”

“…Recently, it has been shown that plant–soil feedback may operate at the intraspecific level, that is, that there are differences in plant growth on own soil compared with growth on soil from different accessions or genotypes within the same species (Bukowski & Petermann, 2014; Liu, Etienne, Liang, Wang, & Yu, 2015). Despite indications that certain pathogens may have similar effects on closely related species (Gilbert, Briggs, & Magarey, 2015; Parker et al., 2015), it is still unclear whether there is a difference in feedback strength between the intraspecific and the interspecific levels (van der Putten et al., 2013). Indeed, there is considerable debate on whether the strength of plant–soil feedback experienced by each plant individual in a community is predictable from information on species relatedness.…”

Effects of Host Variability on the Spread of Invasive Forest Diseases

“…In humans, when transmission of a specialist pathogen is density-dependent, theory predicts a minimal density of the host population below which the pathogen becomes extinct ('crowd disease', [60]). In mixed communities, density-dependent disease dynamics confer an advantage to uncommon species which benefit from a lower enemy pressure ('rare-species advantage'; [61]) and may, therefore, increase in incidence. Examples where host density has affected the spread of an invasive forest pathogen include the beech bark disease involving the exotic beech scale insect Cryptococcus fagisuga Lind.…”

Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

“…This is biologically similar to environments where the plant may be invading a novel habitat that already contain plants that are phylogenetically similar and thus contain herbivores with trait values that match the invading plant. Many studies have found correlations between phylogenetic distance and antagonistic pressures on plants (Pearse and Hipp 2009;Ness et al 2011;Parker et al 2015). The phylogenetic composition of a community may have as great an effect on the outcome of invading plants as the ecological composition.…”