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The genomic signature of rapid coevolution within a wild host-parasite system

Periodic Reporting for period 1 - Coevolution (The genomic signature of rapid coevolution within a wild host-parasite system)

Reporting period: 2019-05-01 to 2021-04-30

Parasites (defined broadly to include viruses, bacteria, protozoans and others) infect nearly all forms of life and act as a powerful force to shape the evolution of host populations and drive the dynamics of biological communities. As host populations evolve in response to their parasites, so too does the parasite evolve in response to its host. This antagonistic coevolution between host and parasite may be responsible for much of the genetic diversity found in natural populations, and is likely a strong driver of local adaptation and population differentiation. Coevolution between host and parasite is also of enormous practical concern for human society, as parasites impose considerable costs in respect to agriculture, livestock production, aquaculture, and human health. In this research, we aim to extend beyond the scope of previous coevolutionary studies and conduct a direct genome-level investigation of antagonistic coevolution between wild populations of a host (Daphnia magna) and its bacterial parasite (Pasteuria ramosa).

This research capitalizes upon recent technical and theoretical advances in the D. magna / P. ramosa model system, and centers upon the measurement of interspecies linkage disequilibrium (here called: interlinkage) across the genomes of both species. Interlinkage is a novel term, which we have defined as a statistical association of alleles across the genomes of separate coevolving species. Although interlinkage has not been formally defined previously, it arises from basic theoretical expectations when coevolutionary dynamics are governed by matching allele interactions (e.g. the likely mode of infection for D. magna / P. ramosa).

Despite arising as a fundamental aspect of some coevolutionary models, interlinkage remains an entirely theoretical construct as it has never been studied within natural populations. This research aims to identify and characterize the signal of interlinkage between wild populations of host (D. magna) and parasite (P. ramosa), and to evaluate this signal across multiple timescales. We expect that these experiments will yield direct genomic evidence of antagonistic coevolution in a natural population, a clear test of Red Queen coevolutionary dynamics, and the first genetic time-series of such resolution and duration. The study of interlinkage will furthermore provide opportunity for the identification of new genomic regions important for some host-parasite interactions.
The primary objective of this research is to find the genomic signature of interlinkage by identifying regions of the P. ramosa and D. magna genomes which are locked in antagonistic coevolution in respect to infectiousness/resistance. We searched for this genomic signature by conducting whole-genome sequencing of host and parasite DNA extracted from 258 naturally infected D. magna from a single wild population. Samples were collected throughout the growing season to ensure that early season and late season genotypes were represented in the data. Host and parasite data were separated in silico by mapping data against reference genomes of both species. In the case of P. ramosa, genetic data were also mapped to a second reference genome produced from isolates endemic to Lake Aegelsee, the source population for our samples. We then developed a custom bioinformatics pipeline to perform a series of co-genome wide association tests (co-GWAS) between the host and parasite genome.

Our preliminary results show a strong statistical signal of interlinkage occurring primarily between a single region of the host genome and a single region of the parasite genome. The identified region in the host genome corresponds a previously characterized region known to contain genes responsible for resistance to P. ramosa infection. The identified region in the parasite genome contains a high density of collagen-like genes, which have previously been hypothesized to play a major role in the P. ramosa infection process. Comparison of the two P. ramosa reference genomes suggest a large degree of structural variation at the highlighted region with possible gene duplications.
The strong signal of interlinkage that we observed between host and parasite genomes provides strong independent confirmation of previous work in the D. magna / P. ramosa system, in which resistance/infection loci were characterized primarily using phenotype data. The independent recovery of these previously identified infection/resistance loci also provides a strong biological validation for our co-GWAS approach. Previous co-GWAS studies have relied upon human clinical data and SNP-chip arrays that represent only a portion of the human genome. Our study is the first to employ co-GWAS methods to full genome data, and the first to examine interlinkage among wild populations. Altogether, our study provides a robust proof of concept for expansion of co-GWAS methodologies to other systems.

The next step in this project will be to construct a genetic time series to examine the temporal dynamics of interlinked loci in Lake Aegelsee P. ramosa / D. magna populations. As the D. magna / P. ramosa system appears to be governed by a matching-allele mechanism, there is a strong theoretical prediction that the frequencies of these coevolving loci will change in frequency together in a closely-associated manner. The observation of such co-changes of host and parasite alleles would provide strong empirical support in favor of this theoretical model. The samples for this aspect of the project were collected in 2019 and 2020, and will be sequenced in the next stage of the project.

After we have reconstructed the short-term temporal dynamics of the interlinked loci, we aim to reconstruct the historical record of antagonistic coevolution between D. magna and P. ramosa across more than 50 years of lake sediment layers. This experiment benefits from the extensive banks of D. magna and P. ramosa resting stages that are deposited in lake sediments. This comparison across time scales is crucial, as previous research in the Lake Aegelsee system indicates that coevolutionary dynamics between D. magna and P. ramosa appear very different when viewed across different sampling intervals. By collecting samples across a much longer timescale, this experiment will illustrate the consequences of selection for the long-term changes to the gene pool, thus making coevolution visible at the genetic level. The sediment cores for this stage of the research have already been collected and are currently preserved in cold storage.
Electron micrograph of the bacteria Pasteuria ramosa. Image courtesy of Dieter Ebert