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.

Plant-mediated CH4 exchange in wetlands: A review of mechanisms and measurement methods with implications for modelling.

Plant-mediated CH4 transport (PMT) is the dominant pathway through which soil-produced CH4 can escape into the atmosphere and thus plays an important role in controlling ecosystem CH4 emission. PMT is affected by abiotic and biotic factors simultaneously, and the effects of biotic factors, such as the dominant plant species and their traits, can override the effects of abiotic factors. Increasing evidence shows that plant-mediated CH4 fluxes include not only PMT, but also within-plant CH4 production and oxidation due to the detection of methanogens and methanotrophs attached to the shoots. Despite the inter-species and seasonal differences, and the probable contribution of within-plant microbes to total plant-mediated CH4 exchange (PME), current process-based ecosystem models only estimate PMT based on the bulk biomass or leaf area index of aerenchymatous plants. We highlight five knowledge gaps to which more research efforts should be devoted. First, large between-species variation, even within the same family, complicates general estimation of PMT, and calls for further work on the key dominant species in different types of wetlands. Second, the interface (rhizosphere-root, root-shoot, or leaf-atmosphere) and plant traits controlling PMT remain poorly documented, but would be required for generalizations from species to relevant functional groups. Third, the main environmental controls of PMT across species remain uncertain. Fourth, the role of within-plant CH4 production and oxidation is poorly quantified. Fifth, the simplistic description of PMT in current process models results in uncertainty and potentially high errors in predictions of the ecosystem CH4 flux. Our review suggest that flux measurements should be conducted over multiple growing seasons and be paired with trait assessment and microbial analysis, and that trait-based models should be developed. Only then we are capable to accurately estimate plant-mediated CH4 emissions, and eventually ecosystem total CH4 emissions at both regional and global scales.

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.

Water level drawdown makes boreal peatland vegetation more responsive to weather conditions.

Climate warming and projected increase in summer droughts puts northern peatlands under pressure by subjecting them to a combination of gradual drying and extreme weather events. The combined effect of those on peatland functions is poorly known. Here, we studied the impact of long-term water level drawdown (WLD) and contrasting weather conditions on leaf phenology and biomass production of ground level vegetation in boreal peatlands. Data were collected during two contrasting growing seasons from a WLD experiment including a rich and a poor fen and an ombrotrophic bog. Results showed that WLD had a strong effect on both leaf area development and biomass production, and these responses differed between peatland types. In the poor fen and the bog, WLD increased plant growth, while in the rich fen, WLD reduced the growth of ground level vegetation. Plant groups differed in their response, as WLD reduced the growth of graminoids, while shrubs and tree seedlings benefited from it. In addition, the vegetation adjusted to the lower WTs, was more responsive to short-term climatic variations. The warmer summer resulted in a greater maximum and earlier peaking of leaf area index, and greater biomass production by vascular plants and Sphagnum mosses at WLD sites. In particular, graminoids benefitted from the warmer conditions. The change towards greater production in the WLD sites in general and during the warmer weather in particular, was related to the observed transition in plant functional type composition towards arboreal vegetation.

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.

After-use of peat extraction sites - A systematic review of biodiversity, climate, hydrological and social impacts.

After drainage for forestry and agriculture, peat extraction is one of the most important causes of peatland degradation. When peat extraction is ceased, multiple after-use options exist, including abandonment, restoration, and replacement (e.g., forestry and agricultural use). However, there is a lack of a global synthesis of after-use research. Through a systematic review of 356 peer-reviewed scientific articles, we address this research gap and examine (1) what after-use options have been studied, (2) what the studied and recognized impacts of the after-use options are, and (3) what one can learn in terms of best practices and research gaps. The research has concentrated on the impacts of restoration (N = 162), abandonment (N = 72), and replacement (N = 94), the latter of which consists of afforestation (N = 46), cultivation (N = 34) and creation of water bodies (N = 14). The studies on abandonment, restoration, and creation of water bodies have focused mostly on analyzing vegetation and greenhouse gas (GHG) fluxes, while the studies assessing afforestation and cultivation sites mostly evaluate the provisioning ecosystem services. The studies show that active restoration measures speed-up vegetation recolonization on bare peat areas, reduce GHG emissions and decrease negative impacts on water systems. The most notable research gap is the lack of studies comparing the environmental and social impacts of the after-use options. Additionally, there is a lack of studies focusing on social impacts and downstream hydrology, as well as long-term monitoring of GHG fluxes. Based on the reviewed studies, a comparison of the impacts of the after-use options is not straightforward. We emphasize a need for comparative empirical research in the extracted sites with a broad socio-ecological and geographical context.

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.

Consistent centennial-scale change in European sub-Arctic peatland vegetation toward Sphagnum dominance-Implications for carbon sink capacity.

Climate warming is leading to permafrost thaw in northern peatlands, and current predictions suggest that thawing will drive greater surface wetness and an increase in methane emissions. Hydrology largely drives peatland vegetation composition, which is a key element in peatland functioning and thus in carbon dynamics. These processes are expected to change. Peatland carbon accumulation is determined by the balance between plant production and peat decomposition. But both processes are expected to accelerate in northern peatlands due to warming, leading to uncertainty in future peatland carbon budgets. Here, we compile a dataset of vegetation changes and apparent carbon accumulation data reconstructed from 33 peat cores collected from 16 sub-arctic peatlands in Fennoscandia and European Russia. The data cover the past two millennia that has undergone prominent changes in climate and a notable increase in annual temperatures toward present times. We show a pattern where European sub-Arctic peatland microhabitats have undergone a habitat change where currently drier habitats dominated by Sphagnum mosses replaced wetter sedge-dominated vegetation and these new habitats have remained relatively stable over the recent decades. Our results suggest an alternative future pathway where sub-arctic peatlands may at least partly sustain dry vegetation and enhance the carbon sink capacity of northern peatlands.

Variation in carbon and nitrogen concentrations among peatland categories at the global scale.

Peatlands account for 15 to 30% of the world's soil carbon (C) stock and are important controls over global nitrogen (N) cycles. However, C and N concentrations are known to vary among peatlands contributing to the uncertainty of global C inventories, but there are few global studies that relate peatland classification to peat chemistry. We analyzed 436 peat cores sampled in 24 countries across six continents and measured C, N, and organic matter (OM) content at three depths down to 70 cm. Sites were distinguished between northern (387) and tropical (49) peatlands and assigned to one of six distinct broadly recognized peatland categories that vary primarily along a pH gradient. Peat C and N concentrations, OM content, and C:N ratios differed significantly among peatland categories, but few differences in chemistry with depth were found within each category. Across all peatlands C and N concentrations in the 10-20 cm layer, were 440 ± 85.1 g kg-1 and 13.9 ± 7.4 g kg-1, with an average C:N ratio of 30.1 ± 20.8. Among peatland categories, median C concentrations were highest in bogs, poor fens and tropical swamps (446-532 g kg-1) and lowest in intermediate and extremely rich fens (375-414 g kg-1). The C:OM ratio in peat was similar across most peatland categories, except in deeper samples from ombrotrophic tropical peat swamps that were higher than other peatlands categories. Peat N concentrations and C:N ratios varied approximately two-fold among peatland categories and N concentrations tended to be higher (and C:N lower) in intermediate fens compared with other peatland types. This study reports on a unique data set and demonstrates that differences in peat C and OM concentrations among broadly classified peatland categories are predictable, which can aid future studies that use land cover assessments to refine global peatland C and N stocks.

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 functional traits play the second fiddle to plant functional types in explaining peatland CO2 and CH4 gas exchange.

Peatlands constitute a significant soil carbon (C) store, yet the C gas flux components show distinct spatial variation both between and within peatlands. Determining the controls on this variability could aid in our understanding of the response of peatlands to global changes. In this study, we assess the usefulness of different vegetation related parameters to explain spatial variation in peatland C gas flux components. We hypothesise that spatial variation is best explained by trait-based indices (similarly to other terrestrial ecosystems), and that the impact of soil physicochemical properties, such as nitrogen (N) content or water level, can be manifested through the traits. Furthermore, we expect that the spatial variability associated with each of the C gas flux components can be explained by a distinct set of traits. To address our aim, we used a successional peatland chronosequence from wet meadows to a bog, along which all variables were recorded with similar methods and under similar climatic conditions. We observed spatial variability with all measured gas fluxes, with carbon dioxide (CO2) fluxes showing significant variability between sites, while within site variability was more important for methane (CH4) fluxes. As expected, our results show that the impacts of physicochemical conditions were directed via vegetation. However, the cover of functional plant types that capture multiple traits proved to be more powerful in explaining gas flux variability compared to functional trait-based indices. Our findings imply that for future gas flux modelling purposes, rather than attempting to use individual traits - as is the ongoing trend in ecology - it might be more useful to refine plant functional groupings and ensure they are based on a set of plant traits relevant for the studied ecosystem process. This could be facilitated by the collation of a large data set of traits measured from peatlands.

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.