The coevolutionary consequences of biodiversity change.

Coevolutionary selection is a powerful process shaping species interactions and biodiversity. Anthropogenic global environmental change is reshaping planetary biodiversity, including by altering the structure and intensity of interspecific interactions. However, remarkably little is understood of how coevolutionary selection is changing in the process. Here, we outline three interrelated pathways - change in evolutionary potential, change in community composition, and shifts in interaction trait distributions - that are expected to redirect coevolutionary selection under biodiversity change. Assessing how both ecological and evolutionary rules governing species interactions are disrupted under anthropogenic global change is of paramount importance to understand the past, present, and future of Earth's biodiversity.

Anna-Liisa Laine.

Interview with Anna-Liisa Laine, who studies the ecology and evolution of plant-microbe interactions at the University of Helsinki.

The evolutionary dynamics of hyperparasites.

Evolutionary theory has typically focused on pairwise interactions, such as those between hosts and parasites, with relatively little work having been carried out on more complex interactions including hyperparasites: parasites of parasites. Hyperparasites are common in nature, with the chestnut blight fungus virus CHV-1 a well-known natural example, but also notably include the phages of important human bacterial diseases. We build a general modeling framework for the evolution of hyperparasites that highlights the central role that the ability of a hyperparasite to be transmitted with its parasite plays in their evolution. A key result is that hyperparasites which transmit with their parasite hosts (hitchhike) will be selected for lower virulence, trending towards hypermutualism or hypercommensalism. We examine the impact on the evolution of hyperparasite systems of a wide range of host and parasite traits showing, for example, that high parasite virulence selects for higher hyperparasite virulence resulting in reductions in parasite virulence when hyperparasitized. Furthermore, we show that acute parasite infection will also select for increased hyperparasite virulence. Our results have implications for hyperparasite research, both as biocontrol agents and for their role in shaping community ecology and evolution and moreover emphasize the importance of understanding evolution in the context of multitrophic interactions.

The first arriving virus shapes within-host viral diversity during natural epidemics.

Viral diversity has been discovered across scales from host individuals to populations. However, the drivers of viral community assembly are still largely unknown. Within-host viral communities are formed through co-infections, where the interval between the arrival times of viruses may vary. Priority effects describe the timing and order in which species arrive in an environment, and how early colonizers impact subsequent community assembly. To study the effect of the first-arriving virus on subsequent infection patterns of five focal viruses, we set up a field experiment using naïve Plantago lanceolata plants as sentinels during a seasonal virus epidemic. Using joint species distribution modelling, we find both positive and negative effects of early season viral infection on late season viral colonization patterns. The direction of the effect depends on both the host genotype and which virus colonized the host early in the season. It is well established that co-occurring viruses may change the virulence and transmission of viral infections. However, our results show that priority effects may also play an important, previously unquantified role in viral community assembly. The assessment of these temporal dynamics within a community ecological framework will improve our ability to understand and predict viral diversity in natural systems.

Plant disease risk is modified by multiple global change drivers.

Plant diseases are strongly influenced by host biodiversity, spatial structure, and abiotic conditions. All of these are undergoing rapid change, as the climate is warming, habitats are being lost, and nitrogen deposition is changing nutrient dynamics of ecosystems with ensuing consequences for biodiversity. Here, I review examples of plant-pathogen associations to demonstrate how our ability to understand, model and predict disease dynamics is becoming increasingly difficult, as both plant and pathogen populations and communities are undergoing extensive change. The extent of this change is influenced via both direct and combined effects of global change drivers, and especially the latter are still poorly understood. Change at one trophic level is expected to drive change also at the other, and hence feedback loops between plants and their pathogens are expected to drive changes in disease risk both through ecological as well as evolutionary mechanisms. Many of the examples discussed here demonstrate an increase in disease risk as a result of ongoing change, suggesting that unless we successfully mitigate global environmental change, plant disease is going to become an increasingly heavy burden on our societies with far-reaching consequences for food security and functioning of ecosystems.

Short-term fitness consequences of parasitism depend on host genotype and within-host parasite community.

Multiparasite communities inhabiting individual hosts are common and often consist of parasites from multiple taxa. The effects of parasite community composition and complexity on host fitness are critical for understanding how host-parasite coevolution is affected by parasite diversity. To test how naturally occurring parasites affect host fitness of multiple host genotypes, we performed a common-garden experiment where we inoculated four genotypes of host plant Plantago lanceolata with six microbial parasite treatments: three single-parasite treatments, a fungal mixture, a viral mixture, and a cross-kingdom treatment. Seed production was affected by both host genotype and parasite treatment, and their interaction jointly determined the growth of the hosts. Fungal parasites had more consistent negative effects than viruses in both single- and mixed-parasite treatments. These results demonstrate that parasite communities have the potential to affect the evolution and ecology of host populations through their effects on host growth and reproduction. Moreover, the results highlight the importance of accounting for the diversity of parasites as well as host genotypes when aiming to predict the consequences of parasites for epidemics as the effects of multiparasitism are not necessarily additive of single-parasite effects, nor uniform across all host genotypes.

Direct and indirect viral associations predict coexistence in wild plant virus communities.

Viruses are a vastly underestimated component of biodiversity that occur as diverse communities across hierarchical scales from the landscape level to individual hosts. The integration of community ecology with disease biology is a powerful, novel approach that can yield unprecedented insights into the abiotic and biotic drivers of pathogen community assembly. Here, we sampled wild plant populations to characterize and analyze the diversity and co-occurrence structure of within-host virus communities and their predictors. Our results show that these virus communities are characterized by diverse, non-random coinfections. Using a novel graphical network modeling framework, we demonstrate how environmental heterogeneity influences the network of virus taxa and how the virus co-occurrence patterns can be attributed to non-random, direct statistical virus-virus associations. Moreover, we show that environmental heterogeneity changed virus association networks, especially through their indirect effects. Our results highlight a previously underestimated mechanism of how environmental variability can influence disease risks by changing associations between viruses that are conditional on their environment.

Intraspecific trait variation and changing life-history strategies explain host community disease risk along a temperature gradient.

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'.

Altered within- and between-host transmission under coinfection underpin parasite co-occurrence patterns in the wild.

Interactions among parasite species coinfecting the same host individual can have far reaching consequences for parasite ecology and evolution. How these within-host interactions affect epidemics may depend on two non-exclusive mechanisms: parasite growth and reproduction within hosts, and parasite transmission between hosts. Yet, how these two mechanisms operate under coinfection, and how sensitive they are to the composition of the coinfecting parasite community, remains poorly understood. Here, we test the hypothesis that the relationship between within- and between-host transmission of the fungal pathogen, Phomopsis subordinaria, is affected by co-occurring parasites infecting the host plant, Plantago lanceolata. We conducted a field experiment manipulating the parasite community of transmission source plants, then tracked P. subordinaria within-host transmission, as well as between-host transmission to naïve recipient plants. We find that coinfection with the powdery mildew pathogen, Podosphaera plantaginis, causes increased between-host transmission of P. subordinaria by affecting the number of infected flower stalks in the source plants, resulting from altered auto-infection. In contrast, coinfection with viruses did not have an effect on either within- or between-host transmission. We then analyzed data on the occurrence of P. subordinaria in 2018 and the powdery mildew in a multi-year survey data set from natural host populations to test whether the positive association predicted by our experimental results is evident in field epidemiological data. Consistent with our experimental findings, we observed a positive association in the occurrence of P. subordinaria and historical powdery mildew persistence. Jointly, our experimental and epidemiological results suggest that within- and between-host transmission of P. subordinaria depends on the identity of coinfecting parasites, with potentially far-reaching effects on disease dynamics and parasite co-occurrence patterns in wild populations. Supplementary Information: The online version contains supplementary material available at 10.1007/s10682-022-10182-9.

Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease.

While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome.

Arbuscular mycorrhizal fungi influence host infection during epidemics in a wild plant pathosystem.

While pathogenic and mutualistic microbes are ubiquitous across ecosystems and often co-occur within hosts, how they interact to determine patterns of disease in genetically diverse wild populations is unknown. To test whether microbial mutualists provide protection against pathogens, and whether this varies among host genotypes, we conducted a field experiment in three naturally occurring epidemics of a fungal pathogen, Podosphaera plantaginis, infecting a host plant, Plantago lanceolata, in the Åland Islands, Finland. In each population, we collected epidemiological data on experimental plants from six allopatric populations that had been inoculated with a mixture of mutualistic arbuscular mycorrhizal fungi or a nonmycorrhizal control. Inoculation with arbuscular mycorrhizal fungi increased growth in plants from every population, but also increased host infection rate. Mycorrhizal effects on disease severity varied among host genotypes and strengthened over time during the epidemic. Host genotypes that were more susceptible to the pathogen received stronger protective effects from inoculation. Our results show that arbuscular mycorrhizal fungi introduce both benefits and risks to host plants, and shift patterns of infection in host populations under pathogen attack. Understanding how mutualists alter host susceptibility to disease will be important for predicting infection outcomes in ecological communities and in agriculture.

Plant biodiversity promotes sustainable agriculture directly and via belowground effects.

While the positive relationship between plant biodiversity and ecosystem functioning (BEF) is well established, the extent to which this is mediated via belowground microbial processes is poorly understood. Growing evidence suggests that plant community structure influences soil microbial diversity, which in turn promotes functions desired for sustainable agriculture. Here, we outline the 'plant-directed' and soil microbe-mediated mechanisms expected to promote positive BEF. We identify how this knowledge can be utilized in plant diversification schemes to maximize ecosystem functioning in agroecosystems, which are typically species poor and sensitive to biotic and abiotic stressors. In the face of resource overexploitation and global change, bridging the gaps between biodiversity science and agricultural practices is crucial to meet food security in the Anthropocene.

Coinfection with a virus constrains within-host infection load but increases transmission potential of a highly virulent fungal plant pathogen.

The trade-off between within-host infection rate and transmission to new hosts is predicted to constrain pathogen evolution, and to maintain polymorphism in pathogen populations. Pathogen life-history stages and their correlations that underpin infection development may change under coinfection with other parasites as they compete for the same limited host resources. Cross-kingdom interactions are common among pathogens in both natural and cultivated systems, yet their impacts on disease ecology and evolution are rarely studied. The host plant Plantago lanceolata is naturally infected by both Phomopsis subordinaria, a seed killing fungus, as well as Plantago lanceolata latent virus (PlLV) in the Åland Islands, SW Finland. We performed an inoculation assay to test whether coinfection with PlLV affects performance of two P. subordinaria strains, and the correlation between within-host infection rate and transmission potential. The strains differed in the measured life-history traits and their correlations. Moreover, we found that under virus coinfection, within-host infection rate of P. subordinaria was smaller but transmission potential was higher compared to strains under single infection. The negative correlation between within-host infection rate and transmission potential detected under single infection became positive under coinfection with PlLV. To understand whether within-host and between-host dynamics are correlated in wild populations, we surveyed 260 natural populations of P. lanceolata for P. subordinaria infection occurrence. When infections were found, we estimated between-hosts dynamics by determining pathogen population size as the proportion of infected individuals, and within-host dynamics by counting the proportion of infected flower stalks in 10 infected plants. In wild populations, the proportion of infected flower stalks was positively associated with pathogen population size. Jointly, our results suggest that the trade-off between within-host infection load and transmission may be strain specific, and that the pathogen life-history that underpin epidemics may change depending on the diversity of infection, generating variation in disease dynamics.

Strain Diversity and Spatial Distribution Are Linked to Epidemic Dynamics in Host Populations.

AbstractThe inherently variable nature of epidemics renders predictions of when and where infection is expected to occur challenging. Differences in pathogen strain composition, diversity, fitness, and spatial distribution are generally ignored in epidemiological modeling and are rarely studied in natural populations, yet they may be important drivers of epidemic trajectories. To examine how these factors are linked to epidemics in natural host populations, we collected epidemiological and genetic data from 15 populations of the powdery mildew fungus, Podosphaera plantaginis, on Plantago lanceolata in the Åland Islands, Finland. In each population, we tracked spatiotemporal disease progression throughout one epidemic season and coupled our survey of infection with intensive field sampling of the pathogen. We found that strain composition varied greatly among populations in the landscape. Within populations, strain composition was driven by the sequence of strain activity: early-active strains reached higher abundances, leading to consistent strain compositions over time. Co-occurring strains also varied in their contribution to the growth of the local epidemic, and these fitness inequalities were linked to epidemic dynamics: a higher proportion of hosts became infected in populations containing strains that were more similar in fitness. Epidemic trajectories in the populations were also linked to strain diversity and spatial dynamics: higher infection rates occurred in populations containing higher strain diversity, while spatially clustered epidemics experienced lower infection rates. Together, our results suggest that spatial and/or temporal variation in the strain composition, diversity, and fitness of pathogen populations are important factors generating variation in epidemiological trajectories among infected host populations.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Genotype-Specific Expression and NLR Repertoire Contribute to Phenotypic Resistance Diversity in Plantago lanceolata.

High levels of phenotypic variation in resistance appears to be nearly ubiquitous across natural host populations. Molecular processes contributing to this variation in nature are still poorly known, although theory predicts resistance to evolve at specific loci driven by pathogen-imposed selection. Nucleotide-binding leucine-rich repeat (NLR) genes play an important role in pathogen recognition, downstream defense responses and defense signaling. Identifying the natural variation in NLRs has the potential to increase our understanding of how NLR diversity is generated and maintained, and how to manage disease resistance. Here, we sequenced the transcriptomes of five different Plantago lanceolata genotypes when inoculated by the same strain of obligate fungal pathogen Podosphaera plantaginis. A de novo transcriptome assembly of RNA-sequencing data yielded 24,332 gene models with N50 value of 1,329 base pairs and gene space completeness of 66.5%. The gene expression data showed highly varying responses where each plant genotype demonstrated a unique expression profile in response to the pathogen, regardless of the resistance phenotype. Analysis on the conserved NB-ARC domain demonstrated a diverse NLR repertoire in P. lanceolata consistent with the high phenotypic resistance diversity in this species. We find evidence of selection generating diversity at some of the NLR loci. Jointly, our results demonstrate that phenotypic resistance diversity results from a crosstalk between different defense mechanisms. In conclusion, characterizing the architecture of resistance in natural host populations may shed unprecedented light on the potential of evolution to generate variation.

The effect of host community functional traits on plant disease risk varies along an elevational gradient.

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.

Effect of maternal infection on progeny growth and resistance mediated by maternal genotype and nutrient availability.

Maternal effects of pathogen infection on progeny development and disease resistance may be adaptive and have important consequences for population dynamics. However, these effects are often context-dependent and examples of adaptive transgenerational responses from perennials are scarce, although they may be a particularly important mechanism generating variation in the offspring of long-lived species.Here, we studied the effect of maternal infection of Plantago lanceolata by Podosphaera plantaginis, a fungal parasite, on the growth, flower production and resistance of the progeny of six maternal genotypes in nutrient-rich and nutrient-poor environments. For this purpose, we combined a common garden study with automated phenotyping measurements of early life stages, and an inoculation experiment.Our results show that the effects of infection on the mother plants transcend to impact their progeny. Although maternal infection decreased total leaf and flower production of the progeny by the end of the growing season, it accelerated early growth and enhanced resistance to the pathogen P. plantaginis.We also discovered that the effects of maternal infection affected progeny development and resistance through a three way-interaction between maternal genotype, maternal infection status and nutrient availability. Synthesis. Our results emphasize the importance of maternal effects mediated through genotypic and environmental factors in long-living perennials and suggest that maternal infection can create a layer of phenotypic diversity in resistance. These results may have important implications for both epidemiological and evolutionary dynamics of host-parasite interactions in the wild.

Agricultural land use disrupts biodiversity mediation of virus infections in wild plant populations.

Human alteration of natural habitats may change the processes governing species interactions in wild communities. Wild populations are increasingly impacted by agricultural intensification, yet it is unknown whether this alters biodiversity mediation of disease dynamics. We investigated the association between plant diversity (species richness, diversity) and infection risk (virus richness, prevalence) in populations of Plantago lanceolata in natural landscapes as well as those occurring at the edges of cultivated fields. Altogether, 27 P. lanceolata populations were surveyed for population characteristics and sampled for PCR detection of five recently characterized viruses. We find that plant species richness and diversity correlated negatively with virus infection prevalence. Virus species richness declined with increasing plant diversity and richness in natural populations while in agricultural edge populations species richness was moderately higher, and not associated with plant richness. This difference was not explained by changes in host richness between these two habitats, suggesting potential pathogen spill-over and increased transmission of viruses across the agro-ecological interface. Host population connectivity significantly decreased virus infection prevalence. We conclude that human use of landscapes may change the ecological laws by which natural communities are formed with far reaching implications for ecosystem functioning and disease.