Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation

Abstract

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs. arms-race dynamics in maintaining polymorphism in natural systems where metapopulation processes predominate. We conducted cross-year epidemiological, infection and genetic studies of multiple wild host and pathogen populations in the Linum-Melampsora association. We observed asynchronous phenotypic fluctuations in resistance and infectivity among demes. Importantly, changes in allelic frequencies at pathogen infectivity loci, and in host recognition of these genetic variants, correlated with disease prevalence during natural epidemics. These data strongly support reciprocal coevolution maintaining balanced resistance and infectivity polymorphisms, and highlight the importance of characterising spatial and temporal dynamics in antagonistic interactions.

Figure 1

Variation in infectivity gene frequencies across years and populations. Sequence analysis of variation at two infectivity loci (AvrP123, AvrP4) was carried out on pathogen isolates used in the glasshouse inoculation study. Two common variants at each Avr locus were identified (AvrP123: Lm-1, Lm-2; AvrP4: Lm-1, Lm-8), although a number of other variants were detected at low frequencies. Frequencies of these variants are shown for each population across years, from 2002 through to 2008.

Figure 2

Variation in pathogen infectivity and host resistance as assessed by glasshouse inoculations. (A) Hosts from 2004, 2006 and 2008 were evaluated against sympatric pathogens from 2002, 2004, 2006 and 2008. Infectivity/resistance (lower infectivity = increased resistance) is shown for contemporary host and pathogen combinations (filled circles) and for hosts infected with pathogens from two years previously (open circles). Color shading in the K and N1 graphs illustrates points used to evaluate cross-year changes in resistance ( =2004–2006; =2006–2008) and infectivity ( =2002–2004; =2004–2006; =2006–2008). (B) Changes in infectivity and resistance between consecutive time periods (see text for details). Significant changes are highlighted (*<0.05, **<0.01, ***<0.001, ****<0.0001; see Table S1).

Figure 3

Changes in pathogen infectivity over time. The infectivity of past, contemporary and future pathogen populations on their sympatric host populations from 2004 (upper panel) and 2006 (lower panel) is plotted.

Figure 4

Frequencies of common pathogen variants for two infectivity loci, AvrP123 and AvrP4, regressed against: a–d) their average infectivity as calculated from the glasshouse inoculation data; and e–h) disease prevalence scored during natural epidemics in the wild host populations for the same years. Variant frequencies were based on molecular analysis of the pathogen isolates collected from hosts infected in the wild (the same isolates used in the glasshouse inoculation trials). Average infectivity was determined using the scores across all years for a given population. Disease prevalence was square-root transformed prior to regression analyses to improve normality (see Methods).

Figure 5

Host lines used in glasshouse inoculations were evaluated for their ability to mount necrotic responses to infiltration with variants of two Avr genes (AvrP123, AvrP4). (A) L. marginale lines N1-06-2008 and K-28-2004 display differential necrotic responses following infiltration with Agrobacterium cultures containing T-DNA plasmids encoding AvrP123 alleles Lm-1 and Lm-5, and AvrP4 alleles Lm-1 and Lm-8. (B–E) Variation in the frequency of resistance reactions to these variants for a subset of host populations for which full data were available. (F) Analysis of the relationship between recognition of AvrP123 alleles and resistance (based on glasshouse inoculations). Hosts showing necrotic reactions to one or both AvrP123 variants were significantly more resistant than hosts that didn’t react (F_{2, 137}=5.33, P=0.0059).