bioRxiv Science⌕ Search

Biology subjects

Zilio, G.

Publications and source records attributed to Zilio, G..

11 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↗

Experimental Evolution of the Thermal Performance Curve

The thermal performance curve (TPC) of an organism captures how population growth depends on temperature. When populations experience increased temperatures, such as during global climate change, one prediction is that their TPC can evolve to accommodate the new environmental temperature. Although studies on TPC evolution have mostly focused on modifications in population growth rates, TPC evolution can be strongly trait-dependent and require a multi-trait analysis. Thus, if and how the entire TPC across a multitude of traits evolves to change its shape in response to increased temperatures remains debated. Here, we empirically tested how the TPCs of multiple demographic, life-history and movement traits can evolve by selecting four freshwater protist species at increased temperatures starting from clonal populations. After one year of selection, populations showed a signature of evolutionary responses to the highest selection temperatures in different traits depending on the species. Particularly, we found consistent evolutionary reductions in body size in the three species having the largest cells and evolved changes in movement behaviour in all species. In contrast, we overall observed little modifications in population growth rate and in the corresponding TPC shape. These results suggest that adaptation, via evolution of TPCs, might involve the concurrent evolution of several traits. However, this may be species-specific and difficult from de-novo mutation alone, suggesting that natural populations that do not have sufficient standing genetic variation might have to be reliant on other means of mitigating the effects of climate change, such as dispersal.

evolutionary biology↗

Identification and characterization of nanobodies acting as molecular chaperones for glucocerebrosidase through a novel allosteric mechanism

The enzyme glucocerebrosidase (GCase) catalyses the hydrolysis of glucosylceramide to glucose and ceramide within lysosomes. Homozygous or compound heterozygous mutations in the GCase-sencoding GBA1 gene cause the lysosomal storage disorder Gaucher disease, while heterozygous mutations are the most frequent genetic risk factor for Parkinsons disease. These mutations commonly affect GCase stability, trafficking or activity. Here, we report the development and characterization of nanobodies (Nbs) targeting and acting as chaperones for GCase. We identified several Nb families that bind with nanomolar affinity to GCase. Based on biochemical characterization, we grouped the Nbs in two classes: Nbs that improve the activity of the enzyme and Nbs that increase GCase stability in vitro. A selection of the most promising Nbs was shown to improve GCase function in cell models and positively impact the activity of the N370S mutant GCase. These results lay the foundation for the development of new therapeutic routes.

biochemistry↗

Evolution of thermal performance curves: a meta-analysis of selection experiments

Temperatures are increasing due to global changes, putting biodiversity at risk. Organisms are faced with a limited set of options to cope with this situation: adapt, disperse or die. We here focus on the first possibility, more specifically, on evolutionary adaptations to temperature. Ectotherms are usually characterized by a hump-shaped relationship between fitness and temperature, a non-linear reaction norm that is referred to as thermal performance curve (TPC). To understand and predict impacts of global change, we need to know whether and how such TPCs evolve. Therefore, we performed a systematic literature search and a statistical meta-analysis focusing on experimental evolution and artificial selection studies. This focus allows us to directly quantify relative fitness responses to temperature selection by calculating fitness differences between TPCs from ancestral and derived populations after thermal selection. Out of 7561 publications screened, we found 47 studies corresponding to our search criteria representing taxa across the tree of life, from bacteria, to plants and vertebrates. We show that, independently of species identity, the studies we found report a positive response to temperature selection. Considering entire TPC shapes, adaptation to higher temperatures traded off with fitness at lower temperatures, leading to niche shifts. Effects were generally stronger in unicellular organisms. By contrast, we do not find statistical support for the often discussed "Hotter is better" hypothesis. While our meta-analysis provides evidence for adaptive potential of TPCs across organisms, it also highlights that more experimental work is needed, especially for under-represented taxa, such as plants and non-model systems.

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↗

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↗

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↗