RESUMEN
Host-associated organisms (i.e., symbionts) commonly interact within their shared hosts to form complex ecological communities. Here we suggest that within-host facilitation, where the presence of one symbiont group promotes establishment, growth, or reproduction of another, is prevalent, can arise from six fundamental mechanisms, and has broad implications for ecosystem dynamics.
RESUMEN
Anthropogenic change is contributing to the rise in emerging infectious diseases, which are significantly correlated with socioeconomic, environmental and ecological factors1. Studies have shown that infectious disease risk is modified by changes to biodiversity2-6, climate change7-11, chemical pollution12-14, landscape transformations15-20 and species introductions21. However, it remains unclear which global change drivers most increase disease and under what contexts. Here we amassed a dataset from the literature that contains 2,938 observations of infectious disease responses to global change drivers across 1,497 host-parasite combinations, including plant, animal and human hosts. We found that biodiversity loss, chemical pollution, climate change and introduced species are associated with increases in disease-related end points or harm, whereas urbanization is associated with decreases in disease end points. Natural biodiversity gradients, deforestation and forest fragmentation are comparatively unimportant or idiosyncratic as drivers of disease. Overall, these results are consistent across human and non-human diseases. Nevertheless, context-dependent effects of the global change drivers on disease were found to be common. The findings uncovered by this meta-analysis should help target disease management and surveillance efforts towards global change drivers that increase disease. Specifically, reducing greenhouse gas emissions, managing ecosystem health, and preventing biological invasions and biodiversity loss could help to reduce the burden of plant, animal and human diseases, especially when coupled with improvements to social and economic determinants of health.
Asunto(s)
Biodiversidad , Cambio Climático , Enfermedades Transmisibles , Contaminación Ambiental , Especies Introducidas , Animales , Humanos , Efectos Antropogénicos , Cambio Climático/estadística & datos numéricos , Enfermedades Transmisibles/epidemiología , Enfermedades Transmisibles/etiología , Conservación de los Recursos Naturales/tendencias , Conjuntos de Datos como Asunto , Contaminación Ambiental/efectos adversos , Agricultura Forestal , Bosques , Especies Introducidas/estadística & datos numéricos , Enfermedades de las Plantas/etiología , Medición de Riesgo , UrbanizaciónRESUMEN
Disease may drive variation in host community structure by modifying the interplay of deterministic and stochastic processes that shape communities. For instance, deterministic processes like ecological selection can benefit species less impacted by disease. When communities have higher levels of disease and disease consistently selects for certain host species, this can reduce variation in host community composition. On the other hand, when host communities are less impacted by disease and selection is weaker, stochastic processes (e.g., drift, dispersal) may play a bigger role in host community structure, which can increase variation among communities. While effects of disease on host community structure have been quantified in field experiments, few have addressed the role of disease in modulating variation in structure among host communities. To address this, we conducted a field experiment spanning three years, using a tractable system: foliar fungal pathogens in an old-field grassland community dominated by the grass Lolium arundinaceum, tall fescue. We reduced foliar fungal disease burden in replicate host communities (experimental plots in intact vegetation) in three fungicide regimens that varied in the seasonal duration of fungicide treatment and included a fungicide-free control. We measured host diversity, biomass, and variation in community structure among replicate communities. Disease reduction generally decreased plant richness and increased aboveground biomass relative to communities experiencing ambient levels of disease. These changes in richness and aboveground biomass were consistent across years despite changes in structure of the plant communities over the experiment's three years. Importantly, disease reduction amplified host community variation, suggesting that disease diminished the degree to which host communities were structured by stochastic processes. These results of experimental disease reduction both highlight the potential importance of stochastic processes in plant communities and reveal the potential for disease to regulate variation in host community structure.
Asunto(s)
Festuca , Fungicidas Industriales , Lolium , Pradera , Biomasa , Poaceae/fisiología , Plantas , Biodiversidad , EcosistemaRESUMEN
Understanding pathogen transmission and infection patterns at multiple biological scales is a central issue in disease ecology and evolution. Here, we suggest that functional traits of host species readily affect infection patterns of species, communities, and landscapes, and thus serve as a linkage for multilevel studies of infectious disease.
Asunto(s)
Ecología , FenotipoRESUMEN
Predicting how climate change will affect disease risk is complicated by the fact that changing environmental conditions can affect disease through direct and indirect effects. Species with fast-paced life-history strategies often amplify disease, and changing climate can modify life-history composition of communities thereby altering disease risk. However, individuals within a species can also respond to changing conditions with intraspecific trait variation. To test the effect of temperature, as well as inter- and intraspecifc trait variation on community disease risk, we measured foliar disease and specific leaf area (SLA; a proxy for life-history strategy) on more than 2500 host (plant) individuals in 199 communities across a 1101 m elevational gradient in southeastern Switzerland. There was no direct effect of increasing temperature on disease. Instead, increasing temperature favoured species with higher SLA, fast-paced life-history strategies. This effect was balanced by intraspecific variation in SLA: on average, host individuals expressed lower SLA with increasing temperature, and this effect was stronger among species adapted to warmer temperatures and lower latitudes. These results demonstrate how impacts of changing temperature on disease may depend on how temperature combines and interacts with host community structure while indicating that evolutionary constraints can determine how these effects are manifested under global change. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.
Asunto(s)
Ecología , Plantas , Humanos , Temperatura , Fenotipo , Hojas de la PlantaRESUMEN
Successful colonization and growth of trees within herbaceous communities may result from different interactions with the herbaceous community. First, colonizing trees compete against larger, established herbs, while subsequent growth occurs among similarly sized or smaller herbs. This shift from colonization to growth may lead three drivers of community dynamics-nutrients, consumers, and herbaceous diversity-to differentially affect tree colonization and, later, tree performance. Initially, these drivers should favor larger, established herbs, reducing tree colonization. Later, when established trees can better compete with herbs, these drivers should benefit trees and increase their performance. In a 4-year study in a southeastern US old field, we added nutrients to, excluded aboveground consumers from, and manipulated initial richness of, the herbaceous community, and then allowed trees to naturally colonize these communities (from intact seedbanks or as seed rain) and grow. Nutrients and consumers had opposing effects on tree colonization and performance: adding nutrients and excluding consumers reduced tree colonization rate, but later increased the size of established trees (height, basal diameter). Adding nutrients and excluding consumers also restricted tree colonization to earlier years of study, which partially explained the effect of nutrient addition on plant size. Together, this shows differing impacts of nutrients and consumers: factors that initially limited tree colonization also resulted in larger established trees. This suggests that succession of grasslands that are either eutrophied or have diminished consumer pressure may experience lags and pulses in woody encroachment, leading to an extended period of herbaceous dominance followed by accelerated woody growth.
Asunto(s)
Plantas , Árboles , Ecosistema , NutrientesRESUMEN
Quantifying the relative impact of environmental conditions and host community structure on disease is one of the greatest challenges of the 21st century, as both climate and biodiversity are changing at unprecedented rates. Both increasing temperature and shifting host communities toward more fast-paced life-history strategies are predicted to increase disease, yet their independent and interactive effects on disease in natural communities remain unknown. Here, we address this challenge by surveying foliar disease symptoms in 220, 0.5 m-diameter herbaceous plant communities along a 1100-m elevational gradient. We find that increasing temperature associated with lower elevation can increase disease by (1) relaxing constraints on parasite growth and reproduction, (2) determining which host species are present in a given location, and (3) strengthening the positive effect of host community pace-of-life on disease. These results provide the first field evidence, under natural conditions, that environmental gradients can alter how host community structure affects disease.
Climate change is causing shifts in the ecology and biodiversity of different world regions at unprecedented rates. Global warming is also linked with changes in the risk for certain infectious diseases in humans, but also in animals and plants. There are several possible mechanisms for this. For one thing, changing weather patterns may affect how pathogens grow and reproduce. For another, the distribution ranges of animal and plant hosts of certain disease-causing pathogens are changing because of global warming. This means that the distributions of pathogens are also changing, and so is the severity of the diseases that they cause. Increasing temperatures may also influence the physiological traits that make host species suitable for pathogens. This is because the traits that allow species to survive or adapt to changes in their environment may also make them better at hosting and transmitting the pathogens that cause disease. For example, in plant communities, rising temperatures could favor species with faster growth rates, quicker reproduction and high dispersal, and these traits are often associated with more efficient spread of disease. Despite a lot of research into the effects of climate, it remains unclear how temperature, pathogen growth and reproduction, and host species' traits and distributions combine and interact to alter infectious disease risk, especially in wild plant communities. To investigate this, Halliday, Jalo and Laine studied an area in southeast Switzerland where natural temperature and biodiversity change gradually through the region. The aim was to explore how relationships between plant biodiversity, pathogens and disease risk change with temperature, and to understand whether environmental or biological factors influence infectious disease risk more. Halliday, Jalo and Laine measured the levels of fungal diseases found in the leaves of plant communities spanning 1,100 meters of elevation, showing that higher temperatures increase disease risk both directly and indirectly. Directly, higher temperatures increased pathogen growth and reproduction, and indirectly, they influenced which plants were present and therefore able to act as disease hosts. The results also indicated that temperature can affect how the traits of plants drive the transmission rates of fungal pathogens. Important predictors of disease risk were traits relating to the growth rate of host plants, which tended to increase in areas with low elevation where the surface of the soil was warm. This study represents the first analysis, in wild plants, of how changing temperatures, the traits of shifting host species, and resident parasite populations interact to impact infectious disease risk. The insights Halliday, Jalo and Laine provided could aid in predicting how global climate change will influence infectious disease risk.
Asunto(s)
Altitud , Biota , Enfermedades de las Plantas/parasitología , Tracheophyta/fisiología , Hojas de la Planta/parasitología , Suelo , Suiza , TemperaturaRESUMEN
Parasites can affect and be affected by the host's microbiome, with consequences for host susceptibility, parasite transmission, and host and parasite fitness. Yet, two aspects of the relationship between parasite infection and host microbiota remain little understood: the nature of the relationship under field conditions, and how the relationship varies among parasites. To overcome these limitations, we performed a field survey of the within-leaf fungal community in a tall fescue population. We investigated how diversity and composition of the fungal microbiome associate with natural infection by fungal parasites with different feeding strategies. A parasite's feeding strategy affects both parasite requirements of the host environment and parasite impacts on the host environment. We hypothesized that parasites that more strongly modify niches available within a host will be associated with greater changes in microbiome diversity and composition. Parasites with a feeding strategy that creates necrotic tissue to extract resources (necrotrophs) may not only have different niche requirements, but also act as particularly strong niche modifiers. Barcoded amplicon sequencing of the fungal ITS region revealed that leaf segments symptomatic of necrotrophs had lower fungal diversity and distinct composition compared to segments that were asymptomatic or symptomatic of other parasites. There were no clear differences in fungal diversity or composition between leaf segments that were asymptomatic and segments symptomatic of other parasite feeding strategies. Our results motivate future experimental work to test how the relationship between the microbiome and parasite infection is impacted by parasite feeding strategy and highlight the potential importance of parasite traits.
Asunto(s)
Microbiota , Micobioma , Parásitos , Enfermedades Parasitarias , Animales , Interacciones Huésped-Parásitos , Microbiota/genética , Parásitos/genéticaRESUMEN
Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to the first infection could generate priority effects among parasites, altering the assembly of later-arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite Podosphaera plantaginis and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population and parasite genotype. Thus, host genotype, spatial structure and priority effects among strains all independently altered parasite assembly. Using a fine-scale survey and sampling of infections on wild hosts in several populations, we then identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within-host priority effects of early-arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.
Asunto(s)
Coinfección , Epidemias , Parásitos , Plantago , Animales , Ascomicetos , HumanosRESUMEN
The dilution effect predicts increasing biodiversity to reduce the risk of infection, but the generality of this effect remains unresolved. Because biodiversity loss generates predictable changes in host community competence, we hypothesised that biodiversity loss might drive the dilution effect. We tested this hypothesis by reanalysing four previously published meta-analyses that came to contradictory conclusions regarding generality of the dilution effect. In the context of biodiversity loss, our analyses revealed a unifying pattern: dilution effects were inconsistently observed for natural biodiversity gradients, but were commonly observed for biodiversity gradients generated by disturbances causing losses of biodiversity. Incorporating biodiversity loss into tests of generality of the dilution effect further indicated that scale-dependency may strengthen the dilution effect only when biodiversity gradients are driven by biodiversity loss. Together, these results help to resolve one of the most contentious issues in disease ecology: the generality of the dilution effect.
Asunto(s)
Biodiversidad , Ecología , Metaanálisis como AsuntoRESUMEN
Host and parasite richness are generally positively correlated, but the stability of this relationship in response to global change remains poorly understood. Rapidly changing biotic and abiotic conditions can alter host community assembly, which in turn, can alter parasite transmission. Consequently, if the relationship between host and parasite richness is sensitive to parasite transmission, then changes in host composition under various global change scenarios could strengthen or weaken the relationship between host and parasite richness. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness in response to global change, we experimentally crossed host diversity (biodiversity loss) and resource supply to hosts (eutrophication), then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post-assembly host species richness, richness-independent host phylogenetic diversity, and colonization by exotic host species. Overall, host richness predicted parasite richness, and as predicted, this effect was moderated by exotic abundance-communities dominated by exotic species exhibited a stronger positive relationship between post-assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness. These results thus provide a novel mechanism to explain how global environmental change can generate contingencies in a fundamental ecological relationship-the positive relationship between host and parasite richness.
Asunto(s)
Parásitos , Animales , Biodiversidad , Eutrofización , Interacciones Huésped-Parásitos , FilogeniaRESUMEN
Lay Summary: Competition often occurs among diverse parasites within a single host, but control efforts could change its strength. We examined how the interplay between competition and control could shape the evolution of parasite traits like drug resistance and disease severity.
RESUMEN
The disease ecology community has struggled to come to consensus on whether biodiversity reduces or increases infectious disease risk, a question that directly affects policy decisions for biodiversity conservation and public health. Here, we summarize the primary points of contention regarding biodiversity-disease relationships and suggest that vector-borne, generalist wildlife and zoonotic pathogens are the types of parasites most likely to be affected by changes to biodiversity. One synthesis on this topic revealed a positive correlation between biodiversity and human disease burden across countries, but as biodiversity changed over time within these countries, this correlation became weaker and more variable. Another synthesis-a meta-analysis of generally smaller-scale experimental and field studies-revealed a negative correlation between biodiversity and infectious diseases (a dilution effect) in various host taxa. These results raise the question of whether biodiversity-disease relationships are more negative at smaller spatial scales. If so, biodiversity conservation at the appropriate scales might prevent wildlife and zoonotic diseases from increasing in prevalence or becoming problematic (general proactive approaches). Further, protecting natural areas from human incursion should reduce zoonotic disease spillover. By contrast, for some infectious diseases, managing particular species or habitats and targeted biomedical approaches (targeted reactive approaches) might outperform biodiversity conservation as a tool for disease control. Importantly, biodiversity conservation and management need to be considered alongside other disease management options. These suggested guiding principles should provide common ground that can enhance scientific and policy clarity for those interested in simultaneously improving wildlife and human health.
Asunto(s)
Biodiversidad , Enfermedades Transmisibles , Ecosistema , Animales , Animales Salvajes , Humanos , Metaanálisis como Asunto , Riesgo , ZoonosisRESUMEN
Diverse host communities commonly inhibit the spread of parasites at small scales. However, the generality of this effect remains controversial. Here, we present the analysis of 205 biodiversity-disease relationships on 67 parasite species to test whether biodiversity-disease relationships are generally nonlinear, moderated by spatial scale, and sensitive to underrepresentation in the literature. Our analysis of the published literature reveals that biodiversity-disease relationships are generally hump-shaped (i.e., nonlinear) and biodiversity generally inhibits disease at local scales, but this effect weakens as spatial scale increases. Spatial scale is, however, related to study design and parasite type, highlighting the need for additional multiscale research. Few studies are unrepresentative of communities at low diversity, but missing data at low diversity from field studies could result in underreporting of amplification effects. Experiments appear to underrepresent high-diversity communities, which could result in underreporting of dilution effects. Despite context dependence, biodiversity loss at local scales appears to increase disease, suggesting that at local scales, biodiversity loss could negatively impact human and wildlife populations.
Asunto(s)
Biodiversidad , Interacciones Huésped-Parásitos , Características de la Residencia , Ecología , Humanos , Modelos Biológicos , Enfermedades Parasitarias/epidemiologíaRESUMEN
High-resource environments typically favor quick-growing, poorly defended plants, while resource-poor environments typically favor slow-growing, well-defended plants. The prevailing hypothesis explaining this pattern states that, as resource availability increases, well-defended, slow-growing species are replaced by poorly defended, fast-growing species. A second hypothesis states that greater resource availability increases allocation to growth at the expense of defense, within species. Regardless of mechanism, if exotic species are released from enemies relative to natives, shifts in allocation to growth and defense both within and among species could differ by geographic provenance. To test whether resource availability alters growth or defense, within and among species, and whether any such effects differ between natives and exotics, we manipulated soil nutrient supply and access of aboveground insect herbivores and fungal pathogens under field conditions to individuals of six native and six exotic grass species that co-occurred in a North Carolina old field. The prevailing hypothesis' prediction-that species-level enemy impact increases with species' nutrient responsiveness-was confirmed. Moreover, this relationship did not differ between native and exotic species. The second hypothesis' prediction-that individual-level enemy impact increases with nutrient supply, after accounting for species-level variation in performance-was not supported. Together, these results support the idea, across native and exotic species, that plant species turnover is the primary mechanism underlying effects of nutrient enrichment on allocation to growth and defense in plant communities.
Asunto(s)
Ecosistema , Poaceae , Animales , Herbivoria , Especies Introducidas , Plantas , SueloRESUMEN
Infectious disease risk is often influenced by host diversity, but the causes are unresolved. Changes in diversity are associated with changes in community structure, particularly during community assembly; therefore, by incorporating change over time, host community assembly may provide a framework to resolve causation. In turn, community assembly can be driven by many processes, including resource enrichment. To test the hypothesis that community assembly causally links host diversity to future disease, we experimentally manipulated host diversity and resource supply to hosts, then allowed communities to assemble for 2 years (surveyed 2012-2014). Initially, host diversity increased disease. Subsequently, host diversity did not directly alter disease. However, host diversity determined the trajectory of host community assembly, altering colonisation by exotic host species and richness-independent host phylogenetic diversity, which together reversed the initial increase in disease. Ultimately, incorporating the temporal dimension of community assembly revealed novel mechanisms linking host diversity to future disease.
Asunto(s)
Biodiversidad , Especificidad del Huésped , Interacciones Huésped-Parásitos , FilogeniaRESUMEN
Parasite epidemics can depend on priority effects, and parasite priority effects can result from the host immune response to prior infection. Yet we lack experimental evidence that such immune-mediated priority effects influence epidemics. To address this research gap, we manipulated key host immune hormones, then measured the consequences for within-host parasite interactions, and ultimately parasite epidemics in the field. Specifically, we applied plant immune-signalling hormones to sentinel plants, embedded into a wild host population, and tracked foliar infections caused by two common fungal parasites. Within-host individuals, priority effects were altered by the immune-signalling hormone, salicylic acid (SA). Scaling up from within-host interactions, hosts treated with SA experienced a lower prevalence of a less aggressive parasite, increased burden of infection by a more aggressive parasite, and experienced fewer co-infections. Together, these results indicate that by altering within-host priority effects, host immune hormones can drive parasite epidemics. This study therefore experimentally links host immune hormones to within-host priority effects and parasite epidemics, advancing a more mechanistic understanding of how interactions among parasites alter their epidemics.
Asunto(s)
Colletotrichum/fisiología , Festuca/inmunología , Interacciones Huésped-Patógeno , Enfermedades de las Plantas/microbiología , Inmunidad de la Planta , Rhizoctonia/fisiología , Ciclopentanos/metabolismo , Festuca/microbiología , Interacciones Huésped-Parásitos , North Carolina , Oxilipinas/metabolismo , Enfermedades de las Plantas/inmunología , Ácido Salicílico/metabolismoRESUMEN
Theory predicts that increasing biodiversity will dilute the risk of infectious diseases under certain conditions and will amplify disease risk under others. Yet, few empirical studies demonstrate amplification. This contrast may occur because few studies have considered the multivariate nature of disease risk, which includes richness and abundance of parasites with different transmission modes. By combining a multivariate statistical model developed for biodiversity-ecosystem-multifunctionality with an extensive field manipulation of host (plant) richness, composition and resource supply to hosts, we reveal that (i) host richness alone could not explain most changes in disease risk, and (ii) shifting host composition allowed disease amplification, depending on parasite transmission mode. Specifically, as predicted from theory, the effect of host diversity on parasite abundance differed for microbes (more density-dependent transmission) and insects (more frequency-dependent transmission). Host diversity did not influence microbial parasite abundance, but nearly doubled insect parasite abundance, and this amplification effect was attributable to variation in host composition. Parasite richness was reduced by resource addition, but only in species-rich host communities. Overall, this study demonstrates that multiple drivers, related to both host community and parasite characteristics, can influence disease risk. Furthermore, it provides a framework for evaluating multivariate disease risk in other systems.
Asunto(s)
Herbivoria , Interacciones Huésped-Parásitos , Insectos/fisiología , Rasgos de la Historia de Vida , Enfermedades de las Plantas/microbiología , Fenómenos Fisiológicos de las Plantas , Plantas/microbiología , Animales , Biodiversidad , Cadena Alimentaria , Pradera , Modelos Biológicos , Análisis Multivariante , North Carolina , Plantas/parasitologíaRESUMEN
Parasite epidemics may be influenced by interactions among symbionts, which can depend on past events at multiple spatial scales. Within host individuals, interactions can depend on the sequence in which symbionts infect a host, generating priority effects. Across host individuals, interactions can depend on parasite phenology. To test the roles of parasite interactions and phenology in epidemics, we embedded multiple cohorts of sentinel plants, grown from seeds with and without a vertically transmitted symbiont, into a wild host population, and tracked foliar infections caused by three common fungal parasites. Within hosts, parasite growth was influenced by coinfections, but coinfections were often prevented by priority effects among symbionts. Across hosts, parasite phenology altered host susceptibility to secondary infections, symbiont interactions and ultimately the magnitude of parasite epidemics. Together, these results indicate that parasite phenology can influence parasite epidemics by altering the sequence of infection and interactions among symbionts within host individuals.
Asunto(s)
Hongos , Interacciones Huésped-Parásitos , Animales , ParásitosRESUMEN
Many factors can promote exotic plant success. Three of these factors-greater pressure from natural enemies on natives, increased soil nutrient supply, and low native species richness-may interact during invasions. To test for independent and interactive effects of these drivers, we planted herbaceous perennial communities at two levels of native richness (monocultures and five-species polycultures). We then factorially manipulated soil nutrient supply and access to these communities by aboveground foliar enemies (fungal pathogens and insect herbivores), and allowed natural colonization to proceed for four years. We predicted that nutrient addition would increase exotic success, while enemy exclusion and increasing native richness would reduce exotic success. Additionally, we expected that enemy exclusion would reduce the benefits of nutrient addition to exotic species most in species-poor communities, and that this effect would be weaker in species-rich communities. In total, we found no evidence that nutrient supply, enemy access, and native richness interacted to influence exotic success. Furthermore, native richness had no effect on exotic success. Instead, nutrient addition increased, and enemy exclusion decreased, exotic success independently. As predicted, enemy exclusion reduced exotic success, primarily by slowing the decline in abundance of planted native species. Together, these results demonstrate that multiple drivers of exotic success can act independently within a single system.