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Experimantal Zoology and Evolution (Ebert)

Projects & Collaborations

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EpiEcoEvo: The role of temperature and transmission route on parasite epidemiological, ecological and evolutionary dynamics

Research Project  | 2 Project Members

Despite their clear importance and potential to broadly influence host populations, little is known about pathogen interactions within a broader ecosystem. This project will use the well-studied Daphnia magna-Pasteuria ramosa as a model host-parasite system to investigate how various factors (temperature, route of transmission and selection for host resistance) interact to influence the repeatable seasonal epidemic dynamics observed in nature in order to further understand the ecological and evolutionary drivers of epidemics. The novelty offered by this project is that it will be using a combination of field observations, mesocosm and laboratory experiments along side with mathematical modelling, aiming to quantify and measure the relative importance of factors that are often recognised to be important for epidemic dynamics. These factors are not well understood, and provide a comprehensive understanding of host-parasite-community dynamics and the ecological, evolutionary and epidemiological processes that govern them. The novelty offered by this project is that it demonstrates interactions between parasites, hosts and other species in the ecosystem, as well as the long-term impact of temperature on host-parasite communities. The combination of different approaches proposed in this project allow us to disentangle the complex relationships between hosts, parasites, the broader ecological community, and the abiotic environment and gain further insight to the rules that govern epidemic cycles and ecological feedback loops. By doing so, it allows to estimate the effect of climate change (in particular warmer summers) on the future dynamics of this host-parasite system. Understanding the drivers of infectious disease dynamics and the complex mechanisms of transmission and their relationship to the biotic and abiotic environment are more important than ever as we face the dual and linked challenges of global change and emerging infectious diseases.

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A genomic perspective on host-parasite coevolution

Research Project  | 1 Project Members

Studies in diverse biological systems have led us to believe that host-parasite coevolution is responsible for the extraordinary genetic diversity seen in some genomic regions, such as MHC genes in jawed vertebrates and R-genes in plants. What is still missing, however, is the functional link between genetic variants for host resistance and parasite infectivity on the level of individual interactions and genomic signatures that are predicted to result from these interactions. In this research proposal-a continuation of my previous SNF grant-I address this topic, focusing on a well-established host-parasite system: the water flea Daphnia magna and its virulent bacterial parasite Pasteuria ramosa. This model system has the potential to reveal the mechanistic connection between resistance and infectivity on the individual level and genomic variation at the species level. Our work may thus serve as a case study for demonstrating how selection on specific host- parasite interactions creates genomic patterns of long-term balancing selection and trans-species polymorphism. The proposed research has three main aims, each with two subprojects (SPs): Aim 1: Identify resistance and infectivity genes: We will use genomic approaches to screen hosts (SP1) and parasites (SP2) for loci related to their interactions, with the overarching aim of understanding how these genes interact to produce phenotypic variation. Specifically, we will map genes for polymorphisms in host resistance and parasite infection using stratified genome-wide association studies (GWAS). Aim 2: Long-term consequences of coevolution: Here we will analyse genomes of D. magna and two related species, D. similis and D. sinensis, for long-term balancing selection and trans-species polymorphism (TSP). SP3 will focus on a known host supergene for resistance, a gene so diverse that it requires a haplotype approach, using long-read sequencing. SP4 will employ candidate-free genome scans to search for signatures of balancing selection and TSP in genotypes of the three species collected over a broad geographic scale. Aim 3: Short-term dynamics of coevolution: Genomes of naturally infected hosts will be sequenced together with those of the infecting parasite. These data will be used to test directly for genetic interactions between host and parasite loci, i.e. interspecies linkage disequilibrium (SP5). Variation at the resulting host and parasite candidate loci will then be tracked over two years in longitudinal samples from a natural population and also in sediment cores taken from the same population (SP6). This will allow us to follow coevolution at the interacting genes over time spans from years to decades. SP6 depends on results from SP5. These subprojects complement each other, promising to create a comprehensive picture of the nature and dynamics of the genes that underlay coevolutionary interactions of this system over both the short-term (via patterns of parasitism and selection) and the long-term (via genomic signatures). The proposed research will close the gap between theory, individual level patterns of disease and genomic signatures at disease loci. This is important not only for this system, but for many other host-parasite systems undergoing antagonistic evolution, including humans and their parasites.

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

Research Project  | 2 Project Members

Parasites infect nearly all forms of metazoan life, and act to shape the evolution of host populations and drive the dynamics of entire biological communities. Parasitism also acts a 2-way street: As host populations evolve in response to selection imposed by their parasites, so too does the parasite evolve in response to its host. This antagonistic coevolution between host and parasite may generate much of the genetic diversity found in natural populations, and is likely a strong driver of local adaptation and population differentiation. Host-parasite coevolution is also of enormous practical concern for human society, as parasites impose considerable costs in respect to agriculture, livestock production, aquaculture, and human health. Unfortunately though, very little empirical evidence is available to evaluate some of the most fundamental predictions of coevolutionary theory, especially in respect to the genomic basis of coevolution, as past studies of antagonistic coevolution have typically been conducted at the phenotypic level, or using simplified host-parasite systems in a laboratory setting. I therefore propose to conduct a direct genomelevel investigation of antagonistic coevolution between wild populations of a host (Daphnia magna) and its bacterial parasite (Pasteuria ramosa). This research will capitalize upon recent technical and theoretical advances in the D. magna / P. ramosa system, and will center upon the measurement of interspecies linkage disequilibrium across the genomes of both species. This investigation will be conducted across multiple timescales: A single point in time, across the course of one year, and across a 50-year sediment core time-series. I 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.

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Testing predictions of Red Queen coevolution

Research Project  | 6 Project Members

Testing predictions of Red Queen coevolution, by Dieter Ebert, Universität Basel SUMMARY It is believed that many biological phenomena (e.g. the evolution of sex, Batesian mimicry, and immune response) have evolved as a consequence of host-parasite coevolution. The leading hypothesis for such coevolution is based on time-lagged negative frequency dependent selection (NFDS), also known as Red Queen coevolution. Evidence from population genetics (e.g. high genetic diversity and balancing selection at disease loci) is consistent with the idea that NFDS drives coevolution in host-parasite systems, but other models of coevolution (e.g., selective sweeps) cannot be easily excluded. Here I propose to test the predictions of the Red Queen coevolution hypothesis by analysis of hosts and parasite dynamics in one well-characterized population. In this Daphnia magna population we observe yearly strong epidemics of the bacterial parasite Pasteuria ramosa. I propose to test the hypothesis that coevolution in this system is driven by NFDS. Subproject A aims to identify the host genes that prevent parasite attachment in one particular population ("The Swisspond"), which has yearly strong epidemics of Pasteuria ramosa. We plan to compare different host-genotypes by sequencing from each resistotype multiple genomes and conduct genome-wide association mapping. In a next step we aim to pinpoint the exact genes responsible for the resistance polymorphism by employing molecular tools (CRISPR/Cas9) to knock down candidate genes in the regions of interest. The cloned offspring of the knock down genotypes will be tested for phenotypic effects in response to multiple parasite clones. Subproject B continues our efforts to find the infectivity genes in the bacterial pathogen Pasteuria. This parasite has now been fully sequenced and genomes from different isolates with known infection characteristics will be compared. As a further step we plan to do a proteomics approach, to identify the proteins which are expressed on the spore surface and which are responsible for the attachment of the parasite to the host. Subproject C aims to uncover the genetic interaction matrix between host and parasite genotypes. Host and parasite isolates from the field will be cloned in the laboratory and the mode of inheritance of resistance will be worked out by conducting genetic crosses among hosts. At the same time, infected hosts will be collected across the course of an epidemic in the field and will be genotypes for candidate genes at host resistance loci and parasite infectivity loci. This "co-genotyping" will allow estimating the strength of genetic host-parasite interactions during natural epidemics and enable us to estimate the strength of selection acting on different genotypes. Expected value of the research: This research aims to provide a convincing case study on the validity and predictions of the Red Queen coevolution hypothesis, offering urgently needed genetic data for theoretical and empirical research in evolution, epidemiology and disease biology. It has implications for our understanding of how coevolution shapes genetic diversity and genomes.

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Testing genetic assumptions and predictions of Red Queen coevolution

Research Project  | 1 Project Members

Testing genetic assumptions and predictions of Red Queen coevolution Grant proposal for the Swiss Nationalfonds by Dieter Ebert, Universität Basel Background : It is believed that many biological phenomena (e.g. the evolution of sex, Batesian mimicry, and immune response) have evolved as a consequence of host-parasite coevolution. The leading hypothesis for such coevolution is based on time-lagged negative frequency dependent selection (NFDS), also known as Red Queen coevolution. Evidence from population genetics (e.g. high genetic diversity and balancing selection at disease loci) is consistent with the idea that NFDS drives coevolution in host-parasite systems, but other models of coevolution (e.g., selective sweeps) cannot be easily excluded. Here I propose to test the specific predictions of Red Queen coevolution by undertaking a genetic analysis of the genes under selection and their evolutionary dynamics, focusing on the genetic interactions of Daphnia magna and its bacterial parasite Pasteuria ramosa . I will test my main hypothesis-that coevolution in this system is driven by NFDS-by exploring the genetic interaction matrix of host and parasite, characterizing the genes involved in these interactions, and tracing their dynamics over a 50-year period in pond sediments that contain layered archives of host and parasite populations. Subproject A aims to uncover the genetic interaction matrix between host and parasite genotypes. We focus on the attachment step of Pasteuria, because polymorphism in attachment genes explains most of Daphnia's variation in resistance. Subproject B aims to identify the host genes that prevent parasite attachment. We have already mapped the location of these genes to a small genomic region. I suggest using association mapping in natural populations to further narrow down this region. Next, we will employ molecular evolution tools to test the prediction that allelic variants at these loci are old and under balancing selection. Furthermore, we will trace temporal changes at the candidate loci and of resistance phenotypes in layered pond sediments that harbour resting stages of host and parasite. This will enable us to observe if there is a signature of fluctuating selection on resistance genes. Subproject C will focus on identifying the infectivity genes in Pasteuria. This parasite shows frequent recombination, allowing us to use a genome-wide approach to analyse genetic diversity in several Pasteuria genomes from different infectotypes (carrying different attachment genes). The candidate regions in the genome will then be tested for associations with the parasite's attachment phenotypes using material from natural populations. Next, the prediction of rapid allele frequency changes will be tested in sediment cores. Finally, we will test the prediction that parasite infectotypes track host resistotypes by combining the sediment core results of Subprojects B and C. Expected value of the research: This research aims to provide a convincing case study on the validity and predictions of the Red Queen coevolution hypothesis, offering urgently needed genetic data for theoretical and empirical research in evolution, epidemiology and disease control. It has implications for our understanding of how coevolution shapes the phenomena related to host-parasite interactions.

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Reassessing the genetic architecture of host-parasite interactions

Research Project  | 1 Project Members

Individuals inevitably vary in both their susceptibility to disease and the severity of disease once an outbreak has occurred. My project is aimed at dissecting the genetic architecture underlying how a host defends against infectious disease and exploring the different strategies host can use to do this, such as resisting infection directly or minimising virulence once a pathogen has invaded. To do so I will combine both QTL mapping and modern quantitative genetic approaches to explore the nature of host-parasite interactions between the crustacean Daphnia magna and it's bacterial parasite Pasteuria ramosa . By extending the work of my previous fellowship and building on these findings with a series of new projects, I aim to identify regions of the host genome that influence the severity of disease, and then link these findings to the broad patterns of genetic variation within and between fitness related traits. This work will highlight how an understanding of both quantitative genetics and life-history trade-offs can generate new insights into the study of host-parasite intersections.

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Loss of heterozygosity during asexual reproduction.

Research Project  | 3 Project Members

Loss of Heterozygosity during Asexual Reproduction Summary Sexual reproduction is a widespread phenomenon in nature. Numerous reviews and theoretical studies have discussed this as a paradoxical situation because everything else being equal, sexual reproduction has high costs. However, the widespread existence and persistence of sexual reproduction combined with the observation that asexual lineages are usually young indicates that sexual reproduction has evolutionary advantages that outweigh its costs. A number of potential advantages have been suggested, among them A) that sexual lineages can purge deleterious mutations more effectively, B) that sexual lineages have a higher potential to evolve in a changing environment, and C) that asexual lines have a lower fitness than commonly expected, because they are faced with an ongoing loss of heterozygosity due to ameiotic recombination. This can occur as either reciprocal (crossover) or nonreciprocal (gene conversion) exchange in apomictic germ-line cells. This latter idea is at the centre of this proposal. Asexual lines often emerge from sexual ancestors, raising the question of why asexuals do not out-compete their sexual relatives. It has been suggested that the loss of heterozygosity (LOH) and its associated loss of fitness may reduce the long-term advantages of asexual reproduction. Recently, LOH has been discovered in asexually reproducing Daphnia. Building on this finding, we here propose two sub-projects to quantify LOH and its fitness consequences during the asexual reproduction of D. magna, taking advantage of recently developed genomic tools. Sub-project A will focus on the estimation of LOH in single generations. Using a high density SNP and INDEL array, we will quantify LOH in several mother-daughter pairs. This approach will not entirely exclude selection: selection during early development against offspring (embryos) with LOH would remain unnoticed. Therefore, we will compliment it with a genome-wide analysis of Mendelian ratios of the codominant markers. Selection against recessive deleterious alleles would distort these ratios and would, in combination with a genetic map, allow us to estimate their number and distribution in the genome. From this one can estimate how much LOH is underestimated due to early selection. Sub-project B will examine the fitness consequences of LOH in asexually propagating lines with and without competition. Furthermore, this project attempts to assess the effect of inbreeding load on LOH under competitive conditions. These experiments will enable us to estimate the longer-term consequences of LOH in asexual populations. This proposed research will provide further insights into the evolution of asexuality, the maintenance of sexual recombination and the genetic mechanisms at work during reproduction. It also promises to increase our understanding of the effects and distributions of deleterious alleles in the genome and of the evolution of genome structure in asexuals.