SLN and SPO conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, and wrote the paper.
The authors have declared that no competing interests exist.
Interactions between hosts and parasites provide an ongoing source of selection that promotes the evolution of a variety of features in the interacting species. Here, we use a genetically explicit mathematical model to explore how patterns of gene expression evolve at genetic loci responsible for host resistance and parasite infection. Our results reveal the striking yet intuitive conclusion that gene expression should evolve along very different trajectories in the two interacting species. Specifically, host resistance loci should frequently evolve to co-express alleles, whereas parasite infection loci should evolve to express only a single allele. This result arises because hosts that co-express resistance alleles are able to recognize and clear a greater diversity of parasite genotypes. By the same token, parasites that co-express antigen or elicitor alleles are more likely to be recognized and cleared by the host, and this favours the expression of only a single allele. Our model provides testable predictions that can help interpret accumulating data on expression levels for genes relevant to host−parasite interactions.
A model reveals that hosts should evolve co-expression of resistance alleles to recognize a range of parasites, but the parasite shouldn't evolve co-expression of infection alleles because it enhances recognition by the host.
Hosts and parasites are locked in a continual co-evolutionary race, which generates
persistent selection for resistant hosts and infectious parasites. Understanding the direct
effects of this process on spatial patterns of local adaptation [
To explore the evolution of expression levels, we assumed that infection/resistance was determined by a single gene in the host with alleles
Determining how expression patterns evolve during the course of host−parasite co-evolution requires that we relate expression patterns to the phenotype expressed by heterozygous genotypes. We assumed that a heterozygous individual of species
For example, the circle corresponds to the additive case, where heterozygotes are equally likely to express either
We incorporated host−parasite co-evolution into the modifier framework described above by considering the following well-studied genetic interactions. In the gene-for-gene (GFG) model [
An Interaction between a Host and a Parasite Results in Either Infection or Resistance, Depending on the Phenotype of the Interacting Species
We assumed a life cycle where selection due to interactions between host and parasite was followed by sexual reproduction. Species interactions are assumed to depend on loci: a regulatory locus with alleles
Genotype frequencies after one round of selection can be determined using standard population genetic equations once the fitnesses of genotypes have been determined. We assume that encounters between species occur at random and that at most one interaction occurs per generation per individual. When interacting with genotype
Thus, we assume that fitness depends upon genotype frequencies but is independent of the population sizes of the interacting species (e.g., [
Assuming an infinite population size and ignoring mutation, we can write down recursions for the frequency,
where primes indicate post-selection genotype
Recursions for the parasite species are identical, with the exceptions of the subscripts
To analyze the model, we assumed that selection was weak relative to the rate of recombination between the modifier locus and the locus determining infection/resistance. This allowed us to derive very general conditions for the evolution of expression levels in the focal species using quasi-linkage equilibrium approximations [
When the host was the focal species, the frequency of allele
where
In
Assuming weak selection,
Similarly, when the parasite was the focal species, the frequency of allele
where now
To the order of these approximations, genetic associations
Examining the signs of
To evaluate whether our analytical results are robust to violations of the assumption that recombination is frequent and selection is weak, we numerically iterated the exact recursions. For each genetic model of co-evolution, we considered both focal hosts and focal parasites, and modifiers that altered the expression probabilities
Taken together, our analytical and simulation results suggest that heterozygous hosts should generally evolve to co-express resistance alleles but heterozygous parasites should evolve to express only a single infection allele (
In both panels, the frequency of a modifier allele that increases the expression of the
Our results demonstrate that co-evolution between hosts and parasites favours co-expression of alleles more often in hosts than in parasites. This predicted pattern is particularly striking among the models with the greatest empirical support (GFG and IMA) and helps explain observed patterns of expression at loci governing infection/resistance in hosts and parasites. Co-expression of resistance alleles has been observed in both the
Although our modelling framework is quite general in many ways, it makes several important assumptions. First, we have assumed that infection and resistance are mediated by a single genetic locus with only two alleles. Adding additional alleles or loci could conceivably alter our results by changing co-evolutionary dynamics in such a way that polymorphism is either more or less likely to be maintained (e.g., [
As we have argued, host−parasite interactions provide a theoretical framework in which to understand and interpret the evolution of genetic systems. While we had previously explored the evolution of ploidy levels in hosts and parasites [
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We thank Aneil Agrawal, Thomas Lenormand, Danny Browning, Mark Dybdahl, Dave Hall, Sylvain Gandon, and an anonymous reviewer for helpful comments. Funding was provided by the National Science Foundation (DEB-0343023 to SLN) and by the Natural Sciences and Engineering Research Council of Canada (to SPO).
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