Abstract Parasites are a major evolutionary force, driving adaptive responses in host populations. Although the link between phenotypic response to parasite-mediated natural selection and the underlying genetic architecture often remains obscure, this link is crucial for understanding the evolution of resistance and predicting associated allele frequency changes in the population. To close this gap, we monitored the response to selection during epidemics of a virulent bacterial pathogen, Pasteuria ramosa, in a natural host population of Daphnia magna. Across two epidemics, we observed a strong increase in the proportion of resistant phenotypes as the epidemics progressed. Field and laboratory experiments confirmed that this increase in resistance was caused by selection from the local parasite. Using a genome wide association study (GWAS), we built a genetic model in which two genomic regions with dominance and epistasis control resistance polymorphism in the host. We verified this model by selfing host genotypes with different resistance phenotypes and scoring their F1 for segregation of resistance and associated genetic markers. Such epistatic effects with strong fitness consequences in host-parasite coevolution are believed to be crucial in the Red Queen model for the evolution of genetic recombination. Usage Notes Data associated to the manuscript: "Ameline C, Bourgeois Y, Vögtli F, Savola E, Engelstädter Y, Andras J, Ebert D. 2020. A two-locus system with strong epistasis underlies rapid parasite-mediated evolution of host resistance. Mol. Biol. Evol. accepted". List of files
################################################################## - Elocus_MBE.R: R script The R script uses the following files: 1. Field monitoring of resistance and prevalence - chh20142015.txt: resistotype and prevalence data for 2014 and 2015 - chhcolorcode.txt: color code for resistotypes - pasteuria_distri_2011: pasteuria genotypes dynamics in 2011 2. Experimental and field infections - experimental_infections.csv: data from experimental infections in 2014 - field_infections.csv: data from field infections in 2015 3. GWAS - orientation.txt: orientation info from reference genome - plink.P1.assoc: association file from SS_S vs. RR_X - plink.P2.assoc: association file from XX_S vs. RR_R - plink.P3.assoc: association file from RR_R vs. RR_S - plink.P4.assoc: association file from SS_S vs. RR_S - plink.P5.assoc: association file from SS_S vs. RR_R 4. genetic crossings data for testing goodness of fit between observed and expected segregation of resistotypes in F1 offspring groups - table0_geno.txt - table0_pheno.txt - table2_geno.txt - table2_pheno.txt - table4_geno.txt - table4_pheno.txt - table5_geno.txt - table5_pheno.txt - table6_geno.txt - table6_pheno.txt - table8_geno.txt - table10_pheno.txt - table11_pheno.txt - DMPR1linkage.txt: data for test linkage of DMPR1 with C locus - DMPR2linkage.txt: data for test linkage of DMPR2 with C locus - DMPR3linkage.txt: data for test linkage of DMPR3 with E locus - DMPR4linkage.txt: data for test linkage of DMPR1 with E locus ##################################################################
Abstract The determinants of variation in a species’ genome-wide nucleotide diversity include historical, environmental, and stochastic aspects. This diversity can inform us about the species’ past and present evolutionary dynamics. In parasites, the mode of transmission and the interactions with the host might supersede the effects of these aspects in shaping parasite genomic diversity. We used genomic samples from 10 populations of the microsporidian parasite Ordospora colligata to investigate present genomic diversity and how it was shaped by evolutionary processes, specifically, the role of phylogeography, co-phylogeography (with the host), natural selection, and transmission mode. Although very closely related microsporidia cause diseases in humans, O. colligata is specific to the freshwater crustacean Daphnia magna and has one of the smallest known eukaryotic genomes. We found an overlapping phylogeography between O. colligata and its host highlighting the long-term, intimate relationship between them. The observed geographic distribution reflects previous findings that O. colligata exhibits adaptations to colder habitats, which differentiates it from other microsporidian gut parasites of D. magna predominantly found in warmer areas. The co-phylogeography allowed us to calibrate the O. colligata phylogeny and thus estimate its mutation rate. We identified several genetic regions under potential selection. Our whole-genome study provides insights into the evolution of one of the most reduced eukaryotic genomes and shows how different processes shape genomic diversity of an obligate parasite.
Habitat instability has an important influence on species' occurrence and community composition. For freshwater arthropods that occur in ephemeral rock pools, the most drastic habitat instabilities are droughts and the intermittent availability of water. However, although the desiccation of a rock pool is detrimental for planktonic populations, it may also bring certain benefits: the exclusion of predators or parasites, for example, or the coexistence of otherwise competitively exclusive species. The commonness of drought resistant resting stages in many aquatic organisms shows the ecological significance of droughts. We measured daily evaporation in 50 rock pools inhabited by three Daphnia species D. magna, D. longispina and D. pulex over one summer. Daily evaporation and ultimately desiccation showed significantly seasonally influenced correlation with pool surface area, presence of vegetation, ambient temperature, wind and standardized evaporation measures. We used the estimates from this analysis to develop a simulation model to predict changes in the water level in 530 individual pools on a daily basis over a 25-year period. Eventually, hydroperiod lengths and desiccation events could be predicted for all of these rock pools. We independently confirmed the validity of this simulation by surveying desiccation events in the 530 rock pools over a whole season in 2006. In the same 530 rock pools, Daphnia communities had been recorded over the 25 years the simulation model considered. We correlated pool-specific occupation lengths of the three species with pool-specific measures of desiccation risk. Occupation lengths of all three Daphnia species were positively correlated with maximum hydroperiod length and negatively correlated with the number of desiccation events. Surprisingly, these effects were not species-specific.
Recombination rate is an essential parameter for many genetic analyses. Recombination rates are highly variable across species, populations, individuals and different genomic regions. Due to the profound influence that recombination can have on intraspecific diversity and interspecific divergence, characterization of recombination rate variation emerges as a key resource for population genomic studies and emphasises the importance of high-density genetic maps as tools for studying genome biology. Here we present such a high-density genetic map for Daphnia magna, and analyse patterns of recombination rate across the genome.A F2 intercross panel was genotyped by Restriction-site Associated DNA sequencing to construct the third-generation linkage map of D. magna. The resulting high-density map included 4037 markers covering 813 scaffolds and contigs that sum up to 77 % of the currently available genome draft sequence (v2.4) and 55 % of the estimated genome size (238 Mb). Total genetic length of the map presented here is 1614.5 cM and the genome-wide recombination rate is estimated to 6.78 cM/Mb. Merging genetic and physical information we consistently found that recombination rate estimates are high towards the peripheral parts of the chromosomes, while chromosome centres, harbouring centromeres in D. magna, show very low recombination rate estimates.Due to its high-density, the third-generation linkage map for D. magna can be coupled with the draft genome assembly, providing an essential tool for genome investigation in this model organism. Thus, our linkage map can be used for the on-going improvements of the genome assembly, but more importantly, it has enabled us to characterize variation in recombination rate across the genome of D. magna for the first time. These new insights can provide a valuable assistance in future studies of the genome evolution, mapping of quantitative traits and population genetic studies.
Understanding the genomic basis of infectious disease is a fundamental objective in co-evolutionary theory with relevance to healthcare, agriculture, and epidemiology. Models of host-parasite co-evolution often assume that infection requires specific combinations of host and parasite genotypes. Co-evolving host and parasite loci are, therefore, expected to show associations that reflect 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 co-evolution among wild populations.
Summary Migration and re‐colonization enable organisms to persist in metapopulations. Re‐colonization success may be limited by the number of arriving migrants or by patch quality. In a well‐studied rock pool Daphnia metapopulation, it is frequently assumed that re‐colonization is limited by the number of arriving migrants, and that all patches are equally suitable for colonization. This assumption strongly influences how observations about dynamics, epidemiology and population genetics for the entire metapopulation are interpreted. Here we test this assumption. In 627 rock pools, we found that high pH , high Ca ++ and high water conductivity were positively correlated with the presence of D. magna . The experimental release of D. magna into randomly chosen natural pools revealed the highest colonization success in pools with high pH . Next, we elevated pH and Ca ++ concentrations in natural pools by adding a system‐specific natural source of calcium carbonate (either from crushed oyster shells or from eider duck droppings, which contain blue mussel shells). These treatments led to a rapid increase in pH and Ca ++ and strongly raised the likelihood that introduced D. magna would establish persistent populations. Therefore, we conclude that low pH and Ca ++ result in unsuitable colonization conditions in two‐thirds of the untreated pools. A further experiment revealed that natural colonization rates were about five times higher in calcium‐treated pools than in untreated pools. Finally, we observed that eider droppings are more frequently found in the catchment area of occupied pools, than they are in those of unoccupied pools, suggesting that the blue mussel shells contained in the eider droppings play an important role in making pools suitable for colonization and in enabling D. magna to persist. Thus, eider ducks are ecosystem engineers in this system. We recalculate typical metapopulation parameters to account for the unsuitable pools, resulting in a much more dynamic picture of this metapopulation than previously believed, with colonization rates and gene flow three to five times higher. These results have strong implications for metapopulation persistence, local and global genetic diversity, genetic rescue, gene flow and local adaptation. Our results emphasize that without verifying patch suitability, estimated rates of metapopulation dynamics can severely underestimate the true rates.
Abstract Although there is little doubt that hosts evolve to reduce parasite damage, little is known about the evolutionary time scale on which host populations may adapt under natural conditions. Here we study the effects of selection by the microsporidian parasite Octosporea bayeri on populations of Daphnia magna. In a field study, we infected replicated populations of D. magna with the parasite, leaving control populations uninfected. After two summer seasons of experimental evolution (about 15 generations), the genetic composition of infected host populations differed significantly from the control populations. Experiments revealed that hosts from the populations that had evolved with the parasite had lower mortality on exposure to parasite spores and a higher competitive ability than hosts that had evolved without the parasite. In contrast, the susceptibility of the two treatment groups to another parasite, the bacterium Pasteuria ramosa , which was not present during experimental evolution of the populations, did not differ. Fitness assays in the absence of parasites revealed a higher fitness for the control populations, but only under low population density with high resource availability. Overall, our results show that, under natural conditions, Daphnia populations are able to adapt rapidly to the prevailing conditions and that this evolutionary change is specific to the environment.
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