Browsing by Subject "LOCAL ADAPTATION"

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  • Peris Tamayo, Ana-Maria; Devineau, Olivier; Praebel, Kim; Kahilainen, Kimmo K.; ostbye, Kjartan (2020)
    Adaptive radiation is the diversification of species to different ecological niches and has repeatedly occurred in different salmonid fish of postglacial lakes. In Lake Tinnsjoen, one of the largest and deepest lakes in Norway, the salmonid fish, Arctic charr (Salvelinus alpinus(L.)), has likely radiated within 9,700 years after deglaciation into ecologically and genetically segregated Piscivore, Planktivore, Dwarf, and Abyssal morphs in the pelagial, littoral, shallow-moderate profundal, and deep-profundal habitats. We compared trait variation in the size of the head, the eye and olfactory organs, as well as the volumes of five brain regions of these four Arctic charr morphs. We hypothesised that specific habitat characteristics have promoted divergent body, head, and brain sizes related to utilized depth differing in environmental constraints (e.g., light, oxygen, pressure, temperature, and food quality). The most important ecomorphological variables differentiating morphs were eye area, habitat, and number of lamellae. The Abyssal morph living in the deepest areas of the lake had the smallest brain region volumes, head, and eye size. Comparing the olfactory bulb with the optic tectum in size, it was larger in the Abyssal morph than in the Piscivore morph. The Piscivore and Planktivore morphs that use more illuminated habitats have the largest optic tectum volume, followed by the Dwarf. The observed differences in body size and sensory capacities in terms of vision and olfaction in shallow and deepwater morphs likely relates to foraging and mating habitats in Lake Tinnsjoen. Further seasonal and experimental studies of brain volume in polymorphic species are needed to test the role of plasticity and adaptive evolution behind the observed differences.
  • Ji, Huawei; Wen, Jiahao; Du, Baoming; Sun, Ningxiao; Berg, Björn; Liu, Chunjiang (2018)
    Key message Foliar phosphorus (P) resorption in Quercus variabilis Blume was significantly lower at a P-rich than at a P-deficient site. Moreover, P resorption strongly decreased, and nitrogen: phosphorus and carbon: phosphorus resorption ratios increased with soil P content. This demonstrates a strong link between foliar P resorption and P content in soils, and emphasizes the importance of P resorption in leaves of trees growing in soils with contrasted P content. Context Subtropical ecosystems are generally characterized by P-deficient soils. However, P-rich soils develop in phosphate rock areas. Aims We compared the patterns of nutrient resorption, in terms of ecological stoichiometry, for two sites naturally varying in soil P content. Methods The resorption efficiency (percentage of a nutrient recovered from senescing leaves) and proficiency (level to which nutrient concentration is reduced in senesced leaves) of 12 elements were determined in two oak (Q. variabilis) populations growing at a P-rich or a P-deficient site in subtropical China. Results P resorption efficiency dominated the intraspecific variation in nutrient resorption between the two sites. Q. variabilis exhibited a low P resorption at the P-rich site and a high P resorption at the P-deficient site. Both P resorption efficiency and proficiency strongly decreased with soil P content only and were positively related to the N:P and C:P ratios in green and senesced leaves. Moreover, resorption efficiency ratios of both N:P and C:P were positively associated with soil P. Conclusion These results revealed a strong link between P resorption and P stoichiometry in response to a P deficiency in the soil, and a single- and limiting-element control pattern of P resorption. Hence, these results provide new insights into the role of P resorption in plant adaptations to geologic variations of P in the subtropics.
  • Booksmythe, Isobel; Gerber, Nina; Ebert, Dieter; Kokko, Hanna (2018)
    Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals' allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia magna. Male production increased with population density, the major ecological driver of sexual reproduction; however, this response was dampened when the population sex ratio was more male-biased. Thus, in line with sex ratio theory, we show that D.magna adjust offspring sex allocation in response to the current population sex ratio.
  • Gerber, Nina; Kokko, Hanna; Ebert, Dieter; Booksmythe, Isobel (2018)
    The timing of sex in facultatively sexual organisms is critical to fitness, due to the differing demographic consequences of sexual versus asexual reproduction. In addition to the costs of sex itself, an association of sex with the production of dormant life stages also influences the optimal use of sex, especially in environments where resting eggs are essential to survive unfavourable conditions. Here we document population dynamics and the occurrence of sexual reproduction in natural populations of Daphnia magna across their growing season. The frequency of sexually reproducing females and males increased with population density and with decreasing asexual clutch sizes. The frequency of sexually reproducing females additionally increased as population growth rates decreased. Consistent with population dynamic models showing that the opportunity cost of sexual reproduction (foregoing contribution to current population growth) diminishes as populations approach carrying capacity, we found that investment in sexual reproduction was highest when asexual population growth was low or negative. Our results support the idea that the timing of sex is linked with periods when the relative cost of sex is reduced due to low potential asexual growth at high population densities. Thus, a combination of ecological and demographic factors affect the optimal timing of sexual reproduction, allowing D. magna to balance the necessity of sex against its costs.
  • Maria del Mar Delgadoa,1,2, Tomas Roslinb,2, Gleb Tikhonovc, Evgeniy Meyked, Coong Loc, Eliezer Gurariee, Marina Abadonovaf, Ozodbek Abduraimovg, Olga Adrianovah, Tatiana Akimovai, Muzhigit Akkievj, Aleksandr Ananink,l, Elena Andreevam, Natalia Andriychukn, Maxim Antipino, Konstantin Arzamascevp, Svetlana Babinaq, Miroslav Babushkinr, Oleg Bakins, Anna Barabancovat, Inna Basilskajau, Nina Belovav, Natalia Belyaevaw, Tatjana Bespalovax, Evgeniya Bisikalovay, Anatoly Bobretsovz, Vladimir Bobrovaa, Vadim Bobrovskyibb, Elena Bochkarevacc,dd, Gennady Bogdanovee, Vladimir Bolshakovff, Svetlana Bondarchukgg, Evgeniya Bukharovak,3, Alena Butuninax, Yuri Buyvolovhh, Anna Buyvolovaii, Yuri Bykovjj, Elena Chakhirevas, Olga Chashchinakk, Nadezhda Cherenkovall, Sergej Chistjakovmm, Svetlana Chuhontsevai, Evgeniy A. Davydovcc,nn, Viktor Demchenkooo, Elena Diadichevaoo, Aleksandr Dobrolyubovpp, Ludmila Dostoyevskayaqq, Svetlana Drovninall, Zoya Drozdovajj, Akynaly Dubanaevrr, Yuriy Dubrovsky...; Kurhinen, Juri (2020)
    For species to stay temporally tuned to their environment, they use cues such as the accumulation of degree-days. The relationships between the timing of a phenological event in a population and its environmental cue can be described by a population-level reaction norm. Variation in reaction norms along environmental gradients may either intensify the envi- ronmental effects on timing (cogradient variation) or attenu- ate the effects (countergradient variation). To resolve spatial and seasonal variation in species’ response, we use a unique dataset of 91 taxa and 178 phenological events observed across a network of 472 monitoring sites, spread across the nations of the former Soviet Union. We show that compared to local rates of advancement of phenological events with the advancement of temperature-related cues (i.e., variation within site over years), spatial variation in reaction norms
  • Tack, Ayco J. M.; Laine, Anna-Liisa (2014)
    •While recent studies have elucidated many of the factors driving parasite dynamics during the growing season, the ecological and evolutionary dynamics during the off-season (i.e. the period between growing seasons) remain largely unexplored. •We combine large-scale surveys and detailed experiments to investigate the overwintering success of the specialist plant pathogen Podosphaera plantaginis on its patchily distributed host plant Plantago lanceolata on the Åland Islands. •Twelve years of epidemiological data establish the off-season as a crucial stage in pathogen metapopulation dynamics, with approximately forty percent of the populations going extinct during the off-season. At the end of the growing season, we observed environmentally-mediated variation in the production of resting structures, with major consequences for spring infection at spatial scales ranging from single individuals to populations within a metapopulation. Reciprocal transplant experiments further demonstrated that pathogen population of origin and overwintering site jointly shaped infection intensity in spring, with a weak signal of parasite adaptation to the local off-season environment. •We conclude that environmentally-mediated changes in the distribution and evolution of parasites during the off-season are crucial for our understanding of host-parasite dynamics, with applied implications for combating parasites and diseases in agriculture, wildlife and human disease systems.
  • Höckerstedt, Layla Maria; Siren, Jukka Pekka; Laine, Anna-Liisa (2018)
    Both theory and experimental evolution studies predict migration to influence the outcome of antagonistic coevolution between hosts and their parasites, with higher migration rates leading to increased diversity and evolutionary potential. Migration rates are expected to vary in spatially structured natural pathosystems, yet how spatial structure generates variation in coevolutionary trajectories across populations occupying the same landscape has not been tested. Here, we studied the effect of spatial connectivity on host evolutionary potential in a natural pathosystem characterized by a stable Plantago lanceolata host network and a highly dynamic Podosphaera plantaginis parasite metapopulation. We designed a large inoculation experiment to test resistance of five isolated and five well-connected host populations against sympatric and allopatric pathogen strains, over 4years. Contrary to our expectations, we did not find consistently higher resistance against sympatric pathogen strains in the well-connected populations. Instead, host local adaptation varied considerably among populations and through time with greater fluctuations observed in the well-connected populations. Jointly, our results suggest that in populations where pathogens have successfully established, they have the upper hand in the coevolutionary arms race, but hosts may be better able to respond to pathogen-imposed selection in the well-connected than in the isolated populations. Hence, the ongoing and extensive fragmentation of natural habitats may increase vulnerability to diseases.
  • Van Belleghem, Steven M.; Vangestel, Carl; De Wolf, Katrien; De Corte, Zoe; Most, Markus; Rastas, Pasi; De Meester, Luc; Hendrickx, Frederik (2018)
    When environments change, populations may adapt surprisingly fast, repeatedly and even at microgeographic scales. There is increasing evidence that such cases of rapid parallel evolution are fueled by standing genetic variation, but the source of this genetic variation remains poorly understood. In the salt-marsh beetle Pogonus chalceus, short-winged 'tidal' and long-winged 'seasonal' ecotypes have diverged in response to contrasting hydrological regimes and can be repeatedly found along the Atlantic European coast. By analyzing genomic variation across the beetles' distribution, we reveal that alleles selected in the tidal ecotype are spread across the genome and evolved during a singular and, likely, geographically isolated divergence event, within the last 190 Kya. Due to subsequent admixture, the ancient and differentially selected alleles are currently polymorphic in most populations across its range, which could potentially allow for the fast evolution of one ecotype from a small number of random individuals, as low as 5 to 15, from a population of the other ecotype. Our results suggest that cases of fast parallel ecological divergence can be the result of evolution at two different time frames: divergence in the past, followed by repeated selection on the same divergently evolved alleles after admixture. These findings highlight the importance of an ancient and, likely, allopatric divergence event for driving the rate and direction of contemporary fast evolution under gene flow. This mechanism is potentially driven by periods of geographic isolation imposed by large-scale environmental changes such as glacial cycles.
  • Weigang, Helene C.; Kisdi, Eva (2015)
    Resources invested in dispersal structures as well as time and energy spent during transfer may often decrease fecundity. Here we analyse an extended version of the Hamilton-May model of dispersal evolution, where we include a fecundity-dispersal trade-off and also mortality between competition and reproduction. With adaptive dynamics and critical function analysis we investigate the evolution of dispersal strategies and ask whether adaptive diversification is possible. We exclude evolutionary branching for concave trade-offs and show that for convex trade-offs diversification is promoted in a narrow parameter range. We provide theoretical evidence that dispersal strategies can monotonically decrease with increasing survival during dispersal. Moreover, we illustrate the existence of two alternative attracting dispersal strategies. The model exhibits fold bifurcation points where slight changes in survival can lead to evolutionary catastrophes. (C) 2015 Elsevier Ltd. All rights reserved.
  • Susi, Hanna; Burdon, Jeremy J.; Thrall, Peter H.; Nemri, Adnane; Barrett, Luke G. (2020)
    A priority for research on infectious disease is to understand how epidemiological and evolutionary processes interact to influence pathogen population dynamics and disease outcomes. However, little is understood about how population adaptation changes across time, how sexual vs. asexual reproduction contribute to the spread of pathogens in wild populations and how diversity measured with neutral and selectively important markers correlates across years. Here, we report results from a long-term study of epidemiological and genetic dynamics within several natural populations of theLinum marginale-Melampsora liniplant-pathogen interaction. Using pathogen isolates collected from three populations of wild flax (L.marginale) spanning 16 annual epidemics, we probe links between pathogen population dynamics, phenotypic variation for infectivity and genomic polymorphism. Pathogen genotyping was performed using 1567 genome-wide SNP loci and sequence data from two infectivity loci (AvrP123,AvrP4). Pathogen isolates were phenotyped for infectivity using a differential set. Patterns of epidemic development were assessed by conducting surveys of infection prevalence in one population (Kiandra) annually. Bayesian clustering analyses revealed host population and ecotype as key predictors of pathogen genetic structure. Despite strong fluctuations in pathogen population size and severe annual bottlenecks, analysis of molecular variance revealed that pathogen population differentiation was relatively stable over time. Annually, varying levels of clonal spread (0-44.8%) contributed to epidemics. However, within populations, temporal genetic composition was dynamic with rapid turnover of pathogen genotypes, despite the dominance of only four infectivity phenotypes across the entire study period. Furthermore, in the presence of strong fluctuations in population size and migration, spatial selection may maintain pathogen populations that, despite being phenotypically stable, are genetically highly dynamic. Author summary Melampsora liniis a rust fungus that infects native flax,Linum marginalein south-eastern Australia where its epidemiology and evolution have been intensively studied since 1987. Over that time, substantial diversity in the pathotypic structure ofM.linihas been demonstrated but an understanding of how genetic diversity in pathogen populations is maintained through space and time is lacking. Here we integrated phenotypic, genotypic and epidemiological datasets spanning 16 annual epidemics across three host populations to examine long-term pathogen genetic dynamics. The results show that host ecotype is the dominant selective force in the face of strong bottlenecks and annual patterns of genetic turnover. Results from previous studies indicate that in this geographic region,M.linilacks the capacity to reproduce sexually-we thus expected to find limited genetic diversity and evidence for strong clonality influencing genetic dynamics within growing seasons. However, the breadth of genomic coverage provided by the SNP markers revealed high levels of genotypic variation withinM.linipopulations. This discovery contrasts with observed phenotypic dynamics as the epidemics of this pathogen were largely dominated by four pathotypes across the study period. Based on a detailed assessment and comparison of pathotypic and genotypic patterns, our study increases the understanding of how genetic diversity is generated and maintained through space and time within wild pathogen populations. The implications for the management of resistance to pathogens in agricultural or conservation contexts are significant: the appearance of clonality may be hiding high levels of pathogen diversity and recombination. Understanding how this diversity is generated could provide new and unique ways to mitigate or suppress the emergence of infectious strains, allowing to efficiently combat harmful diseases.
  • Galindo, Juan; Carvalho, Joao; Sotelo, Graciela; Duvetorp, Marten; Costa, Diana; Kemppainen, Petri; Panova, Marina; Kaliontzopoulou, Antigoni; Johannesson, Kerstin; Faria, Rui (2021)
    Low dispersal marine intertidal species facing strong divergent selective pressures associated with steep environmental gradients have a great potential to inform us about local adaptation and reproductive isolation. Among these, gastropods of the genus Littorina offer a unique system to study parallel phenotypic divergence resulting from adaptation to different habitats related with wave exposure. In this study, we focused on two Littorina fabalis ecotypes from Northern European shores and compared patterns of habitat-related phenotypic and genetic divergence across three different geographic levels (local, regional and global). Geometric morphometric analyses revealed that individuals from habitats moderately exposed to waves usually present a larger shell size with a wider aperture than those from sheltered habitats. The phenotypic clustering of L. fabalis by habitat across most locations (mainly in terms of shell size) support an important role of ecology in morphological divergence. A genome scan based on amplified fragment length polymorphisms (AFLPs) revealed a heterogeneous pattern of differentiation across the genome between populations from the two different habitats, suggesting ecotype divergence in the presence of gene flow. The contrasting patterns of genetic structure between nonoutlier and outlier loci, and the decreased sharing of outlier loci with geographic distance among locations are compatible with parallel evolution of phenotypic divergence, with an important contribution of gene flow and/or ancestral variation. In the future, model-based inference studies based on sequence data across the entire genome will help unravelling these evolutionary hypotheses, improving our knowledge about adaptation and its influence on diversification within the marine realm.
  • Zueva, Ksenia J.; Lumme, Jaakko; Veselov, Alexey E.; Kent, Matthew P.; Primmer, Craig R. (2018)
    Abstract Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.
  • Kotta, Jonne; Vanhatalo, Jarno Petteri; Jänes, Holger; Orav-Kotta, Helen; Rugiu, Luca; Jormalainen, Veijo; Bobsien, Ivo; Viitasalo, Markku; Virtanen, Elina; Nyström Sandman, Antonia; Isaeus, Martin; Leidenberger, Sonja; Jonsson, Per R.; Johannesson, Kerstin (2019)
    Predictive species distribution models are mostly based on statistical dependence between environmental and distributional data and therefore may fail to account for physiological limits and biological interactions that are fundamental when modelling species distributions under future climate conditions. Here, we developed a state-of-the-art method integrating biological theory with survey and experimental data in a way that allows us to explicitly model both physical tolerance limits of species and inherent natural variability in regional conditions and thereby improve the reliability of species distribution predictions under future climate conditions. By using a macroalga-herbivore association (Fucus vesiculosus - Idotea balthica) as a case study, we illustrated how salinity reduction and temperature increase under future climate conditions may significantly reduce the occurrence and biomass of these important coastal species. Moreover, we showed that the reduction of herbivore occurrence is linked to reduction of their host macroalgae. Spatial predictive modelling and experimental biology have been traditionally seen as separate fields but stronger interlinkages between these disciplines can improve species distribution projections under climate change. Experiments enable qualitative prior knowledge to be defined and identify cause-effect relationships, and thereby better foresee alterations in ecosystem structure and functioning under future climate conditions that are not necessarily seen in projections based on non-causal statistical relationships alone.
  • Kulmuni, J.; Westram, A. M. (2017)
    The possibility of intrinsic barriers to gene flow is often neglected in empirical research on local adaptation and speciation with gene flow, for example when interpreting patterns observed in genome scans. However, we draw attention to the fact that, even with gene flow, divergent ecological selection may generate intrinsic barriers involving both ecologically selected and other interacting loci. Mechanistically, the link between the two types of barriers may be generated by genes that have multiple functions (i.e., pleiotropy), and/or by gene interaction networks. Because most genes function in complex networks, and their evolution is not independent of other genes, changes evolving in response to ecological selection can generate intrinsic barriers as a by-product. A crucial question is to what extent such by-product barriers contribute to divergence and speciation-that is whether they stably reduce gene flow. We discuss under which conditions by-product barriers may increase isolation. However, we also highlight that, depending on the conditions (e.g., the amount of gene flow and the strength of selection acting on the intrinsic vs. the ecological barrier component), the intrinsic incompatibility may actually destabilize barriers to gene flow. In practice, intrinsic barriers generated as a by-product of divergent ecological selection may generate peaks in genome scans that cannot easily be interpreted. We argue that empirical studies on divergence with gene flow should consider the possibility of both ecological and intrinsic barriers. Future progress will likely come from work combining population genomic studies, experiments quantifying fitness and molecular studies on protein function and interactions.
  • Kess, Tony; Bentzen, Paul; Lehnert, Sarah J.; Sylvester, Emma V.A.; Lien, Sigbjørn; Kent, Matthew P.; Sinclair-Waters, Marion; Morris, Corey J.; Wringe, Brendan; Fairweather, Robert; Bradbury, Ian R. (2020)
    Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine-scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine-scale adaptation in marine species.
  • Teacher, Amber G. F.; Andre, Carl; Jonsson, Per R.; Merila, Juha (2013)
  • Gyllenberg, Mats; Kisdi, Eva; Weigang, Helene C. (2016)
    Empirical studies of dispersal indicate that decisions to immigrate are patch-type dependent; yet theoretical models usually ignore this fact. Here, we investigate the evolution of patch-type dependent immigration of a population inhabiting and dispersing in a heterogeneous landscape, which is structured by patches of low and high reward. We model the decision to immigrate in detail from a mechanistic underpinning. With the methods of adaptive dynamics, we derive both analytical and numerical results for the evolution of immigration when life-history traits are patch-type dependent. The model exhibits evolutionary branching in a wide parameter range and the subsequent coevolution can lead to a stable coexistence of a generalist, settling in patches of any type, and a specialist that only immigrates into patches of high reward. We find that individuals always settle in the patches of high reward, in which survival until maturation, relative fecundity and emigration probability are high. We investigate how the probability to immigrate into patches of low reward changes with model parameters. For example, we show that immigration into patches of low reward increases when the emigration probability in these patches increases. Further, immigration into patches of low reward decreases when the patches of high reward become less safe during the dispersal season. (C) 2016 Elsevier Ltd. All rights reserved.
  • Parratt, Steven R.; Laine, Anna-Liisa (2018)
    1. The relative importance of bottom-up versus top-down control of population dynamics has been the focus of much debate. In infectious disease biology, research is typically focused on the bottom-up process of host resistance, wherein the direction of control flows from the lower to the higher trophic level to impact on pathogen population size and epidemiology. However, the importance of top-down control by a pathogen's natural enemies has been mostly overlooked. 2. Here, we explore the effects of, and interaction between, host genotype (i.e., genetic susceptibility to pathogen infection) and infection by a hyperparasitic fungus, Ampelomyces spp., on the establishment and early epidemic growth and transmission of a powdery mildew plant pathogen (Podosphaera plantaginis). We used a semi-natural field experiment to contrast the impacts of hyperparasite infection, host-plant resistance and spatial structure to reveal the key factors that determine pathogen spread. We then used a laboratory-based inoculation approach to test whether the field experiment results hold across multiple pathogen-host genetic combinations and to explore hyperparasite effects on the pathogen's later life-history stages. 3. We found that hyperparasite infection had a negligible effect on within-host infection development and between-host spread of the pathogen during the onset of epidemics. In contrast, host-plant resistance was the major determinant of whether plants became infected, and host genotype and proximity to an infection source determined infection severity. 4. Our laboratory study showed that, while the interaction between host and pathogen genotypes was the key determinant of infection outcome, hyperparasitism did, on average, reduce the severity of infection. Moreover, hyperparasite infection negatively influenced the production of the pathogen's overwintering structures. 5. Synthesis and applications. Our results suggest that bottom-up host resistance affects pathogen spread, but top-down control of powdery mildew pathogens is likely more effective against later life-history stages. Further, while hyperparasitism in this system can reduce early pathogen growth under stable laboratory conditions, this effect is not detectable in a semi-natural environment. Considering the effects of hyperparasites at multiple points in pathogen's life history will be important when considering hyperparasite-derived biocontrol measures in other natural and agricultural systems.