Genetic slippage after sex maintains diversity for parasite resistance in a natural host population

Ameline, Camille; Voegtli, Felix; Andras, Jason P.; Dexter, Eric; Engelstädter, Jan; Ebert, Dieter

doi:10.1126/sciadv.abn0051

Cited by 9 publications

(11 citation statements)

References 93 publications

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“…Similarly, model 1 is constrained in such a manner that only within-lineage associations should be observable, which is exactly what the model shows. The C and D loci remain detectable in model 3 (S6, S12 Fig), but show a much weaker signal than the E locus, reflecting previous observations that the E locus appears to be the primary determinant of pasteuria resistance in our study population (Ameline et al 2021; Ameline et al 2022).…”

Section: Discussionsupporting

confidence: 82%

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

Dexter

Fields

Ebert

2022

Preprint

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Understanding the genomic basis of infectious disease is fundamental objective in coevolutionary theory with relevance to healthcare, agriculture, and epidemiology. Models of host-parasite coevolution often assume that infection requires specific combinations of host and parasite genotypes. Coevolving host and parasite loci are therefor expected to show associations that reflects an underlying infection/resistance allele matrix, yet little evidence for such genome-to-genome interactions has been observed among natural populations. We conducted a study to search for this genomic signature across 258 linked host (Daphnia magna) and parasite (Pasteuria ramosa) genomes. Our results show a clear signal of genomic association between multiple epistatically-interacting loci in the host genome, and a family of genes encoding for collagen-like protein in the parasite genome. These findings are supported by laboratory-based infection trials, which show strong correspondence between phenotype and genotype at the identified loci. Our study provides clear genomic evidence of antagonistic coevolution among wild populations.

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Section: Discussionsupporting

confidence: 82%

“…The major differences between these models can be readily interpreted, and to some degree, predicted by the biology of the system. As the E locus loads that the E locus appears to be the primary determinant of pasteuria resistance in our study population (Ameline et al 2021;Ameline et al 2022).…”

Section: Co-gwas Model Differencesmentioning

confidence: 73%

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

Dexter

Fields

Ebert

2022

Preprint

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“…However, fall and winter conditions result in little to no overwintering of D. magna(Ameline et al 2021). In spring, D. magna hatch from resting eggs(Ameline et al 2022). We collected a sample of 102 individuals in the spring of 2017, pool-sequenced, and prepared them for analysis identically to the metapopulation samples.…”

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confidence: 99%

Genetic Drift Shapes the Evolution of a Highly Dynamic Metapopulation

Angst

Ameline

Haag

et al. 2022

Molecular Biology and Evolution

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The dynamics of extinction and (re)colonization in habitat patches are characterizing features of dynamic metapopulations, causing them to evolve differently than large, stable populations. The propagule model, which assumes genetic bottlenecks during colonization, posits that newly founded subpopulations have low genetic diversity and are genetically highly differentiated from each other. Immigration may then increase diversity and decrease differentiation between subpopulations. Thus, older and/or less isolated subpopulations are expected to have higher genetic diversity and less genetic differentiation. We tested this theory using whole-genome pool-sequencing to characterize nucleotide diversity and differentiation in 60 subpopulations of a natural metapopulation of the cyclical parthenogen Daphnia magna. For comparison, we characterized diversity in a single, large, and stable D. magna population. We found reduced (synonymous) genomic diversity, a proxy for effective population size, weak purifying selection, and low rates of adaptive evolution in the metapopulation compared to the large, stable population. These differences suggest that genetic bottlenecks during colonization reduce effective population sizes, which leads to strong genetic drift and reduced selection efficacy in the metapopulation. Consistent with the propagule model, we found lower diversity and increased differentiation in younger and also in more isolated subpopulations. Our study sheds light on the genomic consequences of extinction–(re)colonization dynamics to an unprecedented degree, giving strong support for the propagule model. We demonstrate that the metapopulation evolves differently from a large, stable population and that evolution is largely driven by genetic drift.

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“…Concurrently, as a consequence of natural selection, the proportion of D. magna clones that are susceptible to many locally common parasite strains declines throughout the course of the season, and the proportion of clones that are resistant to many strains increases as the epidemic progresses (Ameline et al 2021). This pattern is repeated yearly, with susceptibility to various strains preserved through overwintering resting eggs and recombination (Ameline et al 2022). The parallel dynamics of P. ramosa prevalence, temperature and D. magna population size in spring prevent us from understanding if P. ramosa outbreaks are limited by temperature, the availability of the susceptible hosts or other factors.…”

Section: The Study Populationmentioning

confidence: 99%

“…In the Swiss Aegelsee pond, D. magna and P. ramosa dynamics have been monitored for the last 10 years (Andras and Ebert 2013, Ameline et al 2021, 2022). The seasonal monitoring includes assessment of prevalence of P. ramosa and D. magna population dynamics and estimates of the proportions of Daphnia ‘resistotypes', i.e.…”

Section: Introductionmentioning

confidence: 99%

The role of temperature in the start of seasonal infectious disease epidemics

Tadiri,

Ebert

2023

Oikos

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Many infectious diseases display strong seasonal dynamics. When both hosts and parasites are influenced by seasonal variables, it is unclear if the start of an epidemic is limited by host or parasite factors or both. The Daphnia–Pasteuria host–parasite system exhibits seasonal epidemics. We aimed to ascertain how temperature contributes to the timing of P. ramosa epidemics in early spring. To this aim, we experimentally disentangled this effect from the effects of temperature on host development and phenology and from that of host traits on parasite time to visible infection. We hypothesized that the parasite is additionally directly limited by low temperatures beyond its need for available hosts. We found that parasite time to visible infection decreased with increasing temperature at a faster rate than host time to hatching and maturity did, consistent with this hypothesis. We also found that hosts hatched from sexual resting stages are less likely to become infected than those produced clonally, and that hosts resistant to many known parasite strains are slower to show signs of visible infection compared to those susceptible to many. Together, these results imply that climate change could lead to earlier seasonal epidemics for this host–parasite system, which may also impact longer‐term population dynamics.

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Genetic slippage after sex maintains diversity for parasite resistance in a natural host population

Cited by 9 publications

References 93 publications

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

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

Genetic Drift Shapes the Evolution of a Highly Dynamic Metapopulation

The role of temperature in the start of seasonal infectious disease epidemics

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