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Kaltz, O.

Publications and source records attributed to Kaltz, O..

15 recordsLinked to original sources

Differing effects of parasite-parasite interaction types on the spatial epidemiology of co-circulating parasites

Interactions among co-circulating parasite species influence infection risk and disease progression. Interactions can occur within hosts, e.g. altering susceptibility, or indirectly through host demography or movement, potentially affecting landscape-scale transmission. Despite their ubiquity, the spatial implications of these interactions have received limited attention. We combine spatially-explicit modelling with laboratory experiments to investigate how parasite-parasite interactions influence disease spread. We model within-host, demographic, and dispersal-related interactions across a linear landscape, showing that within-host interactions modifying host susceptibility have the strongest effects on parasite prevalence, spatial heterogeneity, and rate of spread. These effects are amplified when parasites invade sequentially, generating pronounced patch-level priority effects. We tested these predictions experimentally using a protist host (Paramecium caudatum) and two bacterial parasites (Holospora undulata and H. obtusa). Consistent with model predictions, we found that H. obtusa reduces the overall prevalence and spread of H. undulata across a landscape of interconnected patches, likely through reductions in host susceptibility, and evidence of priority effects, observing reduced H. undulata prevalence when introduced after H. obtusa. Our results highlight that parasite-parasite interactions can have important implications for the landscape-scale epidemiology of co-circulating parasites, but the effect magnitude depends on the interaction type and the timing of invasion.

ecology↗

Evolution at experimental epidemic fronts speeds up parasite spread

Spreading epidemics can foster the rapid emergence of novel parasite variants. Similar to range expansions, parasites at the front of an epidemic wave may evolve traits facilitating their spatial spread. Typically, higher transmissibility and virulence are expected to evolve at the epidemic front, but predictions change if virulence reduces dispersal of infected hosts. We investigated the feedbacks between epidemiology and evolution in interconnected microcosms of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. First, two long-term treatments mimicked the moving front of epidemic waves, with and without the natural dispersal of infected hosts. Phenotypic trait assays revealed an eco-to-evo feedback: front parasites (i.e., travelling with infected hosts) were less virulent and interfered less with host dispersal, but also showed higher infectivity, compared to parasites from the control treatment. Whole-genome resequencing and analyses of functional genomic diversity corroborated such phenotypic divergence. Second, measurement of the spread of evolved parasites in linear landscapes demonstrated an evo-to-eco feedback: front parasites produced stronger infection outbreaks and faster spreading epidemic waves than did control parasites. A simulation model assessed the relative importance of the different parasite traits in determining infectious spread over a broad parameter range. It suggests that, if dispersal is generally low, higher infectivity alone can produce the observed differences in epidemic spread speed. Our study illustrates how the need to travel with the host shapes eco-evolutionary feedbacks at parasite invasion fronts, and it highlights the importance of considering concomitant evolutionary change when predicting epidemic speed. Significance StatementWhen predicting disease spread across spatial scales it is fundamental to consider host dispersal, but also the concomitant evolution of parasite traits such as infectivity and virulence. We tested how dispersal constraints affect parasite evolution and epidemic spread in an aquatic model system, by combining experimental evolution, genetic analysis and mathematical modelling. Our results suggest that epidemics can be accelerated by the evolution of highly infectious, but not necessarily more virulent parasites, in contrast to conventional views. This illustrates the important role of eco-evolutionary feedback loops can play in shaping the spread of emerging or geographically expanding parasites.

evolutionary biology↗

Environmental complexity constrains evolutionary adaptation across taxa

Complex environments combining multiple stressors are the new norm worldwide. Adaptive evolution will be critical to population persistence under these combined challenges, but how environmental complexity affects the pace of evolution remains poorly understood. Using a meta-experimental evolution approach, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors and their pairwise combinations for multiple generations, while keeping the overall stress level comparable. Populations evolving under combined stressors tended to have lower fitness increase in the selective environments, higher fitness reductions in the control environment, and shallower relation between initial maladaptation and fitness gain, than under single stressors. However, these responses varied with species and stressor type. Accounting for such constraints on evolutionary dynamics should prove crucial for the management of biodiversity. Significance StatementA pressing challenges for modern science and society in the face of ongoing global change is understanding what limits the capacity of living organisms to adapt to complex environments combining multiple stressors. To answer to this question, we conducted a large-scale meta-experimental evolution design across a diversity of organisms, exposing them for multiple generations to either single or combined-stress treatments. Combined stressors led to less adaptive fitness gain than single stressors, and imposed additional costs through reduced fitness in non-stressful conditions. This unique combination of meta-experimental approach with a careful distinction between environmental complexity and overall stress allowed us to gain robust quantitative evidence on how environmental complexity can impact the pace of evolution.

evolutionary biology↗

Co-evolution of host dispersal and parasite virulence in complex landscapes.

Spatial network structure impacts the ecological and evolutionary dynamics of species interactions. Previous work on host-parasite systems has shown that parasite virulence is driven by dispersal rates and spatial structure, assuming that dispersal is an ecologically fixed parameter. However, dispersal is also a trait under selection and can evolve. In this context, we develop an individual-based eco-evolutionary model, in which both parasite virulence and host dispersal can evolve in representative terrestrial (random-geometric graphs; RGGs) and riverine aquatic (optimal channel networks; OCNs) landscapes. We find that in riverine aquatic landscapes, evolutionarily stable (ES) dispersal rates are lower and ES virulence is greater relative to terrestrial landscapes when dispersal mortality is low. When dispersal mortality is high, both dispersal and virulence evolve to lower values in both landscape types. Diverging co-evolutionary patterns between landscapes are explained by differences in network topology. Specifically, the highly heterogeneous degree distribution in riverine aquatic landscapes 1) leads to low parasite relatedness allowing for the evolution of greater virulence and 2) leads to spatial heterogeneity in host densities that constrains the evolution of dispersal to lower values. Our work highlights the importance of considering the concurrent and co-evolution of dispersal when studying trait evolution in complex landscapes.

evolutionary biology↗

Landscape structure drives eco-evolution in host-parasite systems.

Spatial network structure of biological systems drives ecology and evolution by distributing organisms and their genes. The ubiquitous host-parasite systems are no exception. However, past work has largely ignored relevant spatial complexity, hampering the translation of theoretical predictions to real ecosystems. Thus, we develop an eco-evolutionary metapopulation model of host-parasite dynamics where hosts and parasites disperse through realistically complex spatial networks representing major biomes: riverine aquatic and terrestrial. We generate the testable prediction that parasite virulence, or how parasites harm their hosts, is unimodal with dispersal and can reach greater values in aquatic landscapes but saturates to lower values in terrestrial systems. Moreover, we show that kin selection drives virulence evolution. Spatial networks generate characteristic patterns of parasite relatedness which drive differential virulence evolution. Finally, we show that accounting for virulence evolution allows us to predict the distribution of key epidemiological variables (e.g., parasite extinction risks) within spatial networks.

evolutionary biology↗

Predicting evolution in experimental range expansions of an aquatic model system

Predicting range expansion dynamics is a challenge for both fundamental and applied research in conservation and global change biology. However, if ecological and evolutionary processes occur on the same time scale, predictions are challenging to make. Combining experimental evolution and mathematical modelling, we assessed the predictability of independent realisations of range expansions in a laboratory model system, the freshwater protozoan Paramecium caudatum. We followed ecological dynamics and evolutionary change in range core and front populations in the experiment. These settings were recreated in a predictive mathematical model, parametrized with dispersal and growth data of the of the 20 founder strains in the experiment. We find that short-term evolution was driven by selection for increased dispersal at the front and general selection for higher growth rates in all treatments. There was a good quantitative match of predicted and observed trait changes. Phenotypic divergence was mirrored by a complete genotypic divergence, indicating the highly repeatable fixation of strains that also were the most likely winners in our model. Long-term evolution in the experimental range front lines resulted in the emergence of a dispersal syndrome, namely a competition - colonisation trade-off. Altogether, both model and experiment highlight the importance of dispersal evolution as a driver of range expansions. Our study suggests that evolution at range fronts may follow predictable trajectories, at least for simple scenarios, and that predicting these dynamics may be possible from knowledge of few key parameters.

evolutionary biology↗

Phylogeography of infectious disease: genetic diversity and connectivity of the Ostreid herpesvirus 1 population in France

The genetic diversity of viral populations is a key driver of the spatial and temporal diffusion of viruses; yet, studying the diversity of whole genomes from natural populations still remains a challenge. Phylodynamic approaches are commonly used for RNA viruses harboring small genomes, but have only rarely been applied to DNA viruses with larger genomes. Here, we used the Pacific Oyster Mortality Syndrome (POMS, a disease that affects oyster farms around the world) as a model to study the genetic diversity of its causative agent, the Ostreid herpesvirus 1 (OsHV-1) in the three main French oyster-farming areas. Using ultra-deep sequencing on individual moribund oysters and an innovative combination of bioinformatics tools, we de novo assembled 21 OsHV-1 new genomes. Combining quantification of major and minor genetic variations, phylogenetic analysis and ancestral state reconstruction of discrete traits approaches; we assessed the connectivity of OsHV-1 viral populations between the three oyster-farming areas. Our results suggest that the Marennes- Oleron Bay represents the main source of OsHV-1 diversity, from where the virus has dispersed to other farming areas, a scenario consistent with current practices of oyster transfers in France. We demonstrate that phylodynamic approaches can be applied to aquatic DNA viruses to determine how epidemiological, immunological, and evolutionary processes act and potentially interact to shape their diversity patterns. ImportancePhylogeography is a field of research that attempts to reconstruct the relationships between individual genotypes within a species and then correlate these genealogical relationships with their geographic and temporal origin. This field of research has become an essential step in the understanding of pandemics, in particular to determine the origin, spread and evolution of a pathogen as currently illustrated in studies on viral pandemics. However, because phylogeographic analyses are based on genome variation, stable genomes yield less information than labile genomes. Accordingly, viruses with double-stranded DNA (dsDNA) genomes generally have lower nucleotide diversity than RNA viruses. In this study, by combining the use of both major and minor genetic variations with phylogeographic analyses of the oyster herpesvirus OsHV-1, we highlight genealogical relationships that are not depicted in phylogenetic trees based on consensus viral genomes only. These data offer a plausible scenario reflecting the origin and spread of OsHV-1 populations between oyster- farming sites.

microbiology↗

Heritable variation in resistance to the endonuclear parasite Holospora undulata across clades of Paramecium caudatum

Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of genetic variation in this trait can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative genetic variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains (with broad-sense heritability > 0.5), repeatable between laboratories and ranging from total resistance to near-complete susceptibility. Early (one week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2-3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural genetic variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.

genetics↗

Genetic variation in dispersal plasticity in an aquatic host-parasite model system

Dispersal is a central determinant of spatial dynamics in communities and ecosystems, and various ecological factors can shape the evolution of constitutive and plastic dispersal behaviours. One important driver of dispersal plasticity is the biotic environment. Parasites, for example, influence the internal condition of infected hosts and define external patch quality. Thus state-dependent dispersal may be determined by infection status and context-dependent dispersal by the abundance of infected hosts in the population. A prerequisite for such dispersal plasticity to evolve is a genetic basis on which natural selection can act. Using interconnected microcosms, we investigated dispersal in experimental populations of the freshwater protist Paramecium caudatum in response to the bacterial parasite Holospora undulata. For a collection of 20 natural host strains, we found substantial variation in constitutive dispersal, and to a lesser degree in dispersal plasticity. First, infection tended to increase or decrease dispersal relative to uninfected controls, depending on strain identity, potentially indicative of state-dependent dispersal plasticity. Infection additionally decreased host swimming speed compared to the uninfected counterparts. Second, for certain strains, there was a weak negative association between dispersal and infection prevalence, such that uninfected hosts tended to disperse less when infection was more frequent in the population, indicating context-dependent dispersal plasticity. Future experiments may test whether the observed differences in dispersal plasticity are sufficiently strong to react to natural selection. The evolution of dispersal plasticity as a strategy to mitigate parasite effects spatially may have important implications for epidemiological dynamics.

evolutionary biology↗

Host-parasite dynamics set the ecological theatre for the evolution of state- and context-dependent dispersal in hosts

While host-parasite interactions are ubiquitous, the large scale consequences of parasite infections are mainly driven by the spatial context. One trait of pivotal importance for the eco-evolutionary dynamics of such metapopulations is the spatial behaviour of hosts, that is, their dispersal. It is well established that dispersal is not a random process, rather dispersal is informed and may depend on internal and external factors. In host-parasite metapopulations, dispersal may be a function of a hosts infection state, but also of the local context, such as host density or parasite prevalence. Using a dynamical host-parasite metapopulation model, we explore whether host dispersal evolves to be state- and context-dependent and what shapes the evolutionarily stable dispersal reaction norms have. We show that state-dependent dispersal readily evolves in the sense that hosts disperse more when infected. This dispersal bias evolves due to kin selection which is consistent with previous studies. Most importantly, we show that prevalence-dependent dispersal evolves, especially when virulence is high and epidemiological dynamics have predictable signatures. The observed evolutionary outcome, a negatively prevalence-dependent dispersal reaction norm for susceptible hosts, seems counter-intuitive at first. However, our results can be readily explained by the emergent epidemiological dynamics, especially their spatial and temporal correlation patterns. Finally, we show that context-dependency in dispersal may rely on both, prevalence, but also host density cues. Our work provides new insights into the evolution of complex dispersal phenotypes in host-parasite metapopulations as well as on associated feedbacks between ecological dynamics and evolutionary change.

evolutionary biology↗

Trade-off between virulence and dispersal drives parasite evolution at experimental invasion front

Eco-evolutionary processes may play an important role in the spatial spread of infectious disease. Current theory predicts more exploitative parasites to evolve in highly connected populations or at the front of spreading epidemics. However, many parasites rely on host dispersal to reach new populations. This may lead to conflict between local transmission and global spread, possibly counteracting selection for higher virulence. Here, we used the freshwater host Paramecium caudatum and its bacterial parasite Holospora undulata to investigate parasite evolution under an experimental range expansion scenario with natural host dispersal. We find that parasites evolving at experimental range fronts favoured higher dispersal rates of infected hosts than did parasites evolving in core populations. Front parasites further showed lower levels of virulence (host division and survival) and delayed development of infection, consistent with parameter estimates from an epidemiological model that we fitted on experimental time-series data. This combined evidence suggests an evolutionary trade-off between virulence and host-mediated dispersal, with a concomitant reduction in the investment into horizontal transmission. Our experiment illustrates how parasite evolution can be shaped by divergent selection encountered in different segments of an epidemic wave. Such an interplay between demography and spatial selection has important implications for the understanding and management of emerging diseases, and, more generally, for biological invasions and other non-equilibrium scenarios of spreading populations. SIGNIFICANCE STATEMENTWhat drives parasite evolution in spatially expanding epidemics? Many parasites require dispersal of infected hosts to reach new patches, and this may produce specific adaptations enhancing spatial spread. We performed experimental range expansions in an aquatic model system, with natural dispersal of infected hosts. Parasites from experimental range fronts were less virulent and interfered less with host dispersal, but also invested less in horizontal transmission than parasites from the range core. Thus, dispersal adaptation at the front may come at a cost of reduced horizontal transmission, a trade-off rarely considered in theoretical models on parasite virulence evolution. These results have important implications in the context of emerging diseases, and for parasite evolution during biological invasions or other spatial non-equilibrium scenarios.

evolutionary biology↗

Travelling with a parasite: the evolution of resistance and dispersal syndrome during experimental range expansion

Rapid evolutionary change during range expansions can lead to diverging range core and front populations, with the emergence of dispersal syndromes (coupled responses in dispersal and life-history traits). Besides intraspecific effects, range expansions may be impacted by interspecific interactions such as parasitism. Yet, despite the potentially large impact of parasites imposing additional selective pressures on the host, their role on range expansions remains largely unexplored. Using microcosm populations of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata, we studied experimental range expansions under parasite presence or absence. We found that the interaction of range expansion and parasite treatments affected the evolution of host dispersal syndromes. Namely, front populations showed different associations of population growth parameters and swimming behaviours than core populations, indicating divergent evolution. Parasitism reshaped trait associations, with hosts evolved in the presence of the parasite exhibiting overall increased resistance and reduced dispersal. Nonetheless, when comparing infected range core and front populations, we found a positive association, suggesting joint evolution of resistance and dispersal at the front. We conclude that host-parasite interactions during range expansions can change evolutionary trajectories; this in turn may feed back on the ecological dynamics of the range expansion and parasite epidemics.

evolutionary biology↗

When enemies do not become friends: Experimental evolution of heat-stress adaptation in a vertically transmitted parasite

Strict vertical (parent-to-offspring) transmission of symbionts may be associated with benevolence and mutualism, because host reproduction and symbiont transmission are linked. Nonetheless, many such symbionts do reduce host fitness costs and the factors driving their evolution are unclear. Using microcosm populations of Caedibacter taeniospiralis, a vertically transmitted bacterial symbiont of the protozoan Paramecium tetraurelia, we investigated evolutionary change under permissive conditions (26{degrees}C) and under heat stress (32{degrees}C), over 150 host generations. We found evidence for symbiont adaptation to heat stress, involving increased infection persistence and, consequently, higher rates of vertical transmission. For certain genetic backgrounds, heat-stress adaptation was associated with higher proliferation of infected lines at 26{degrees}C, suggesting cost-free evolution of super-generalists. Despite a general decrease in symbiont virulence relative to ancestral strains, infected evolved lines still showed substantial reductions (>20%) in population growth. There was no sign of a temperature-specific reduction in virulence or protection of the host against heat stress. Our results show that obligately vertically transmitted symbionts can still qualify as parasites and evolve adaptations that do not help their hosts. Long-term infection persistence might require additional mechanisms, such as the symbiont-mediated killer trait in this system, allowing the selective elimination of uninfected individuals in the population.

evolutionary biology↗

Phage steering of antibiotic-resistance evolution in the bacterial pathogen Pseudomonas aeruginosa

Antimicrobial resistance is a growing global concern and has spurred increasing efforts to find alternative therapeutics. Bacteriophage therapy has seen near constant use in eastern Europe since its discovery over a century ago. One promising approach is to use phages that not only reduce bacterial pathogen loads, but also select for phage resistance mechanisms that trade-off with antibiotic resistance - so called phage steering. Recent work has shown that phage OMKO1 can interact with efflux pumps and in so doing select for both phage resistance and antibiotic sensitivity. We tested the robustness of this approach to three different antibiotics in vitro and one in vivo. We show that in vitro OMKO1 can reduce antibiotic resistance either in the absence or the presence of antibiotics. Our in vivo experiment showed that phage increased the survival times of wax moth larvae and increased bacterial sensitivity to erythromycin, both in the absence and presence of the antibiotic. We discuss the implications of our findings for future research on this promising therapeutic approach using OMKO1.

evolutionary biology↗

Bottom-up and top-down control of dispersal across major organismal groups: a coordinated distributed experiment

Organisms rarely experience a homogeneous environment. Rather, ecological and evolutionary dynamics unfold in spatially structured and fragmented landscapes, with dispersal as the central process linking these dynamics across spatial scales. Because dispersal is a multi-causal and highly plastic life-history trait, finding general drivers that are of importance across species is challenging but highly relevant for ecological forecasting.\n\nWe here tested whether two fundamental ecological forces and main determinants of local population dynamics, top-down and bottom-up control, generally explain dispersal in spatially structured communities. In a coordinated distributed experiment spanning a wide range of actively dispersing organisms, from protozoa to vertebrates, we show that bottom-up control, that is resource limitation, consistently increased dispersal. While top-down control, that is predation risk, was an equally important dispersal driver as bottom-up control, its effect depended on prey and predator space use and whether dispersal occurred on land, in water or in the air: species that routinely use more space than their predators showed increased dispersal in response to predation, specifically in aquatic environments. After establishing these general causes of dispersal, we used a metacommunity model to show that bottom-up and top-down control of dispersal has important consequences for local population fluctuations as well as cascading effects on regional metacommunity dynamics. Context-dependent dispersal reduced local population fluctuations and desynchronized dynamics between communities, two effects that increase population and community stability.\n\nOur study provides unprecedented insights into the generality of the positive resource dependency of dispersal as well as a robust experimental test of current theory predicting that predator-induced dispersal is modulated by prey and predator space use. Our experimental and theoretical work highlights the critical importance of the multi-causal nature of dispersal as well as its cascading effects on regional community dynamics, which are specifically relevant to ecological forecasting.

ecology↗