Abstract
Properties encompassed by host-pathogen interaction networks have potential to give valuable insight into the evolution of specialization and coevolutionary dynamics in host-pathogen interactions. However, network approaches have been rarely utilized in previous studies of host and pathogen phenotypic variation. Here we applied quantitative analyses to eight networks derived from spatially and temporally segregated host (Linum marginale) and pathogen (Melampsora lini) populations. First, we found that resistance strategies are highly variable within and among networks, corresponding to a spectrum of specialist and generalist resistance types being maintained within all networks. At the individual level, specialization was strongly linked to partial resistance, such that partial resistance was effective against a greater number of pathogens compared to full resistance. Second, we found that all networks were significantly nested. There was little support for the hypothesis that temporal evolutionary dynamics may lead to the development of nestedness in host-pathogen infection networks. Rather, the common patterns observed in terms of nestedness suggests a universal driver (or multiple drivers) that may be independent of spatial and temporal structure. Third, we found that resistance networks were significantly modular in two spatial networks, clearly reflecting spatial and ecological structure within one of the networks. We conclude that (1) overall patterns of specialization in the networks we studied mirror evolutionary trade-offs with the strength of resistance; (2) that specific network architecture can emerge under different evolutionary scenarios; and (3) network approaches offer great utility as a tool for probing the evolutionary and ecological genetics of host-pathogen interactions.
Highlights
Interactions between wild hosts and their pathogens are typically characterized by high levels of genetic diversity for partner specificity, such that pathogens vary in their capacity to infect individual hosts, and hosts are likewise variable in their ability to resist attack by individual pathogens (Laine et al, 2011; Tack et al, 2012)
We found that host resistance strategies are consistently variable within and among networks, corresponding to a spectrum of specialists and generalists being maintained within all networks
While we hypothesized that temporal evolutionary dynamics might be important for the development of nestedness in host-pathogen infection networks, there was little evidence to suggest that this was so
Summary
Interactions between wild hosts and their pathogens are typically characterized by high levels of genetic diversity for partner specificity, such that pathogens vary in their capacity to infect individual hosts, and hosts are likewise variable in their ability to resist attack by individual pathogens (Laine et al, 2011; Tack et al, 2012). Polymorphisms for resistance and infectivity in wild host– pathogen interactions are typically measured by performing pair-wise infections of host lines by pathogens isolated from natural populations. The results of such pair-wise infections can be represented as a matrix or bipartite network (see Box 1 for description), where the rows indicate host genotypes, the columns indicate pathogen genotypes, and the cells within the matrix indicate whether a given combination results in resistance or infectivity. Nestedness is a network property describing the extent to which specialists interact with a subset of partners that interact with generalists, whereas modularity indicates the extent to which resistance or infectivity interactions can be partitioned into distinct groups, each of which has many internal interactions but few with other groups (see Box 1 for a detailed description of these key statistical properties)
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