Phylogenetic structure and host abundance drive disease pressure in communities

• Published in: Nature (London) Vol. 520; no. 7548; pp. 542 - 544
• Main Authors: Parker, Ingrid M., Saunders, Megan, Bontrager, Megan, Weitz, Andrew P., Hendricks, Rebecca, Magarey, Roger, Suiter, Karl, Gilbert, Gregory S.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23-04-2015; Nature Publishing Group
• Subjects: 13/1; 13/95; 14/19; 631/158/1469; 631/158/2178; 631/158/853; 631/449/2668; 64/116; 96/1; 96/95; Biodiversity; California; Databases, Factual; Diseases and pests; Environmental aspects; Epidemiology; Flowers & plants; Genetic aspects; Grassland; Grasslands; Horticulture; Host-parasite relationships; Humanities and Social Sciences; Identification and classification; Introduced species; Introduced Species - trends; letter; multidisciplinary; Pathogenic microorganisms; Pathogens; Phylogenetics; Phylogeny; Plant communities; Plant diseases; Plant Diseases - statistics & numerical data; Plants - classification; Population Density; Rare species; Relative abundance; Science; Threatened species; California; United States
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14372

Rare species may have an advantage in a community by suffering less from disease; here it is shown that, because pathogens are shared among species, it is not just the abundance of a particular species but the structure of the whole community that affects exposure to disease.
Rare species' disease risk
One advantage that rare species have in a community is that they may suffer less from disease — and pathogen pressure increases as a host species becomes more abundant. In a study of a Californian grassland habitat, Ingrid Parker
et al
. demonstrate that the structure of the whole community also influences exposure to disease. They show that plants suffer more disease when they have evolutionarily close species around them, reflecting the fact that many pathogens can attack several species, and as they move from host to host they tend to favour species that are closely related. The authors develop a model to predict the incidence of disease in different species of plants in natural communities, and successfully predict the degree of disease pressure on newly introduced plant species. They also show that this phylogenetically distant species advantage might contribute to the invasiveness of introduced species.
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
,
4
,
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.