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Host–parasite co-evolution and its genomic signature

Abstract

Studies in diverse biological systems have indicated that host–parasite co-evolution is responsible for the extraordinary genetic diversity seen in some genomic regions, such as major histocompatibility (MHC) genes in jawed vertebrates and resistance genes in plants. This diversity is believed to evolve under balancing selection on hosts by parasites. However, the mechanisms that link the genomic signatures in these regions to the underlying co-evolutionary process are only slowly emerging. We still lack a clear picture of the co-evolutionary concepts and of the genetic basis of the co-evolving phenotypic traits in the interacting antagonists. Emerging genomic tools that provide new options for identifying underlying genes will contribute to a fuller understanding of the co-evolutionary process.

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Fig. 1: Schematic representation of selective sweep co-evolution in the gene pools of a host and parasite population.
Fig. 2: Temporal dynamics of genomic signatures.
Fig. 3: Host resistotype and parasite infectotype interaction matrix and balancing selection.
Fig. 4: Idealized scenario for host–parasite co-evolution by long-term balancing selection leading to trans-species polymorphisms.
Fig. 5: Co-genomic approaches to find genes involved in host–parasite interactions.

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Acknowledgements

The authors thank the Ebert laboratory for fruitful discussion and S. Zweizig for comments on the language of the manuscript. This work is supported by a grant from the Swiss National Science Foundation.

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Glossary

Parasites

Organisms, including pathogens, that take advantage of other organisms (hosts), thereby instigating a process of selection by the host to defend against the parasite.

Genomic signatures

Characteristic patterns of genetic variation, observed at a genomic region in a sample of genomes.

Selective sweep

The spread of a beneficial mutant and the hitch-hiking of genetic variants close to it in the genome. Beneficial mutants may have arisen de novo or were segregating in the population before the sweep and become beneficial after a change in conditions.

Balancing selection

Selection that occurs because the alleles involved have, on average, a selective advantage that correlates negatively with their frequency within a population or species. This term does not include loci that are at a balance between gaining and losing variants, such as mutation-drift and mutation-selection balance.

Linked selection

The evolution of (nearly) neutral SNPs influenced by selection on loci physically linked to them.

Genetic hitch-hiking

The process by which a genetic variant changes in frequency because it is physically linked to another variant that is changing in frequency due to selection.

Co-genomic

The simultaneous analysis of the function, structure and evolution of pairs of associated genomes in closely interacting organisms, such as host and parasites.

Overdominance

The scenario in which heterozygotes have a more extreme phenotypic trait value than all homozygotes. Overdominance for fitness results in balancing selection for the alleles causing the advantage for the heterozygote genotypes.

Local adaptation

If the effect of an allele is habitat-specific, such that it is beneficial in one habitat and detrimental in another, and vice versa for the alternative allele, local adaptation may evolve with directional selection within each population. Local adaption is a powerful mechanism to maintain genetic diversity within species.

Direct negative frequency-dependent selection

The selective benefit of an allele depends directly and negatively on its frequency, for example at sex-determining loci and plant self-incompatibility loci.

Indirect negative frequency-dependent selection

The selective benefit of an allele depends on the frequency of an allele in a co-evolving species.

Selective interference

In clonal, but not in sexual, populations, beneficial mutations interfere with each other, such that at a given moment the fittest mutation will outcompete weaker beneficial mutations. Interference can also affect the spread of mutants in genomic regions with low recombination rates.

Linkage disequilibrium

A statistical measure of the distribution of combinations of alleles at different loci, which is zero if this distribution follows the expectation based only on allele frequencies. Non-zero values of linkage disequilibrium can arise due to hitch-hiking, selection on allele combinations and stochastic processes, and may occur among loci without physical linkage.

Selection coefficient

A measure of fitness of genotypes or alleles relative to a reference, such as the ancestral form.

Tajima’s D

A population genetic summary statistic describing the frequency distribution of polymorphisms in a population, with D being zero under neutral evolution and positive under balancing selection.

Genetic drift

A neutral evolutionary process that influences allele frequencies based on the random sampling of genetic variants during reproduction.

Panmictic

Random mating within a population.

Fixation index

A measure of genetic differentiation of spatially structured populations, usually estimated from SNP or microsatellite data.

Directional selection

A mode of natural selection by which a genetic variant is predicted to spread to fixation (also known as positive selection).

Supergene

A group of tightly linked genes on a chromosome that are inherited together as a haplotype and often have reduced recombination.

Functional guilds

Groups of organisms with similar lifestyle characteristics that perform the same ecological function, such as gut parasites, pollinators and filter-feeders.

R-gene

Resistance genes of plants that convey resistance against diseases by producing R proteins.

Approximate Bayesian computation

A Bayesian statistical approach wherein parameter inference and model selection are conducted in the absence of likelihood functions. Instead, approximate Bayesian computation relies on summary statistics and simulations to infer posterior distributions of parameters and/or models of interest.

Likelihood function

The analytical formulation of a set of parameters that can be used to assess the fit of a given observed data set to a predetermined model.

Supervised machine learning

Machine learning is a statistical methodology that uses artificial intelligence to automate inferential processes with minimal explicit instruction. Supervised machine learning is a type of machine learning that uses (labelled) training sets to generate a target function when the correspondence between the function of interest and the response variable is known. This target function can then be applied to unclassified (unlabelled) data to make statistical inferences.

Ancestral recombination graph

(ARG). A genealogical or phylogenetic representation of the network of coalescence and recombination events in a collection of orthologous DNA sequences.

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Ebert, D., Fields, P.D. Host–parasite co-evolution and its genomic signature. Nat Rev Genet 21, 754–768 (2020). https://doi.org/10.1038/s41576-020-0269-1

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