Uncovering the genomic basis of infection through co-genomic sequencing of hosts and parasites

Dexter, Eric; Fields, Peter D.; Ebert, Dieter

doi:10.1101/2022.12.05.519109

Cited by 3 publications

(4 citation statements)

References 52 publications

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“…We were able to confirm the Illumina genotypes and the presence of a plausible number of heterozygous positions surrounding all our candidates (examples of chromatograms in Supplementary Figs. [19][20][21][22][23][24].…”

Section: Population Genetic Analysis Of Shared Polymorphismsmentioning

confidence: 99%

“…A system with strong evidence of Red Queen coevolution is the planktonic crustacean Daphnia magna and its obligate and highly virulent bacterial pathogen Pasteuria ramosa. In this system, coevolution has been associated with high diversity at disease loci [20][21][22] , with resistance being highly variable within and between host populations [21][22][23] . The same is true for parasite infectivity 20,24 .…”

mentioning

confidence: 99%

“…The same is true for parasite infectivity 20,24 . Genomic regions containing resistance loci in hosts and infectivity loci in the parasites show strongly elevated diversity levels compared to the genomic background 22 . Variation in hosts and parasites is linked by high specificity, such that infection can only result when host and parasite genotypes match 22,25,26 , an important assumption of the Red Queen model and long-term balancing selection 27,28 .…”

mentioning

confidence: 99%

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Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Cornetti,

Fields,

Du Pasquier

et al. 2024

Nat Commun

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Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms that predate speciation events are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms may occur. Trans-species polymorphisms have been identified for loci related to mating systems and the MHC, but they are generally rare. Trans-species polymorphisms in disease loci are believed to be a consequence of long-term host-parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scan the genomes of three crustaceans with a divergence of over 15 million years and identify 11 genes containing identical-by-descent trans-species polymorphisms with the same polymorphisms in all three species. Four of these genes display molecular footprints of balancing selection and have a function related to immunity. Three of them are located in or close to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of trans-species polymorphisms for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years.

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Section: Population Genetic Analysis Of Shared Polymorphismsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Cornetti,

Fields,

Du Pasquier

et al. 2024

Nat Commun

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“…These highly dynamic interactions generate and maintain genetic diversity among and within populations. A few genomic regions coding for genes of the host's immune system show evidence of parasite-mediated balancing selection and consequently maintain remarkably high levels of polymorphism (Dexter et al, 2023;Eizaguirre & Lenz, 2010). This is particularly true for the genes of the major histocompatibility complex (MHC).…”

Section: Introductionmentioning

confidence: 99%

Expression diversity of cichlid MHC alleles

Bracamonte,

Hablützel,

Lozano-Martín

et al. 2024

Preprint

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Diversification by natural selection is a major source of biodiversity. The selective pressures imposed by parasites on their hosts have the potential to increase diversity at immunologically relevant genes and maintain high polymorphism within and among populations. The immune genes of the major histocompatibility complex (MHC) are a hallmark of parasite-mediated selection. These genes frequently show local adaptation to the prevailing parasites. Although associations between parasites and alleles have been identified, they are often imperfect, indicating that parasite-mediated selection goes beyond sequence identity. Here, we explored allele-specific expression of MHC class IIB in cichlid fish and its relationship with sequence diversity. This revealed a few highly abundant alleles with consistently low expression, and many relatively rare alleles with high expression levels that were variable among individuals. Alleles that formed functional supertypes also had similar expression. This suggests that rare alleles may be those responding to parasites and that similar functionality may be provided by different alleles in different individuals. Our results further suggest that there could be an optimal number of MHC alleles per individual and that deviations from this optimum are compensated by adjusting expression levels. The common and lowly expressed alleles may have attained different functions, a patterns that appears to be consistent in Neotropical and African cichlids. Our study shows that MHC expression is highly variable among alleles potentially interacting with parasites, providing an additional substrate for selection. Furthermore, our study exemplifies how combining genetic diversity with detailed expression information can help identifying functionally relevant diversity.

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Inference of host-pathogen interaction matrices from genome-wide polymorphism data

Märkle,

John,

Metzger

et al. 2023

Preprint

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Coevolution is defined as the evolutionary change in one antagonist (host) in response to changes in the other antagonist (pathogen). At the genetic level, these changes are determined by genotype x genotype (GxG) interactions. We build on a general theoretical model of a host-pathogen interaction to derive four indices to retrieve key features of GxG interactions. The four developed indices extract relevant information from polymorphism data of randomly sampled uninfected hosts as well as infected hosts and their respective pathogen strains. Using these indices as summary statistics in an Approximate Bayesian Computation method, we can show their power to discriminate between GxG interaction matrices. Second, we apply our ABC method to a SNP data set of 451 European humans and their infecting Hepatitis C Virus (HCV) strains supplemented by polymorphism data of 503 individuals from the 1,000 genomes project. As our indices encompass and extend previous natural co-GWAs we recover many of the associations previously reported for this dataset and infer their underlying interaction matrix. We reveal a new candidate gene for resistance to HCV in the human genome, and two groups of significant GxG associations exhibiting gene-for-gene interactions. We suggest that the inferred types of GxG interactions result from the recent expansion, adaptation and low prevalence of the HCV virus population in Europe.

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Uncovering the genomic basis of infection through co-genomic sequencing of hosts and parasites

Cited by 3 publications

References 52 publications

Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Expression diversity of cichlid MHC alleles

Inference of host-pathogen interaction matrices from genome-wide polymorphism data

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