Landscape heterogeneity shapes host‐parasite interactions and results in apparent plant–virus codivergence

Knowledge on how landscape heterogeneity shapes host–parasite interactions is central to understand the emergence, dynamics and evolution of infectious diseases. However, this is an underexplored subject, particularly for plant–virus systems. Here, we analyse how landscape heterogeneity influences the prevalence, spatial genetic structure, and temporal dynamics of Pepper golden mosaic and Pepper huasteco yellow vein begomoviruses infecting populations of the wild pepper Capsicum annuum glabriusculum (chiltepin) in Mexico. Environmental heterogeneity occurred at different nested spatial scales (host populations within biogeographical provinces), with levels of human management varying among host population within a province. Results indicate that landscape heterogeneity affects the epidemiology and genetic structure of chiltepin‐infecting begomoviruses in a scale‐specific manner, probably related to conditions favouring the viruses' whitefly vector and its dispersion. Increased levels of human management of the host populations were associated with higher virus prevalence and erased the spatial genetic structure of the virus populations. Also, environmental heterogeneity similarly shaped the spatial genetic structures of host and viruses. This resulted in the congruence between host and virus phylogenies, which does not seem to be due to host‐virus co‐evolution. Thus, results provide evidence of the key role of landscape heterogeneity in determining plant–virus interactions.     

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.     

Long‐term variation in environmental conditions influences host–parasite fitness

Long‐term data on host and parasite fitness are important for predicting how host–parasite interactions will be altered in an era of global change. Here, we use data collected from 1997 to 2013 to explore effects of changing environmental conditions on bird–blowfly interactions in northern New Mexico. The objectives of this study were to examine what climate variables influence blowfly prevalence and intensity and to determine whether blowflies and climate variables affect bird fledging success. We examined how temperature, precipitation, and drought affect two parasitic blowflies and their hosts, Western Bluebirds (Sialia mexicana) and Ash‐throated Flycatchers (Myiarchus cinerascens). We found that blowfly prevalence did not change over time. Blowfly intensity increased over time in bluebird nests, but not in flycatcher nests. More blowflies result in slightly higher fledging success in bluebirds, but not flycatchers. There was a significant interaction between blowflies and precipitation on bluebird fledging success. For flycatchers, there was a significant interaction between blowflies and temperature and between blowflies and drought severity on fledging success. Given that the southwest is projected to be hotter and have more frequent and prolonged droughts, we predict that flycatchers may be negatively impacted by blowflies if these trends continue. Future work should focus on investigating the role of both blowflies and climate on fledging success. Climate patterns may negatively impact host fitness through altered parasite pressure.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

Genome‐wide association studies on the phyllosphere microbiome: Embracing complexity in host–microbe interactions

Environmental sequencing shows that plants harbor complex communities of microbes that vary across environments. However, many approaches for mapping plant genetic variation to microbe‐related traits were developed in the relatively simple context of binary host–microbe interactions under controlled conditions. Recent advances in sequencing and statistics make genome‐wide association studies (GWAS) an increasingly promising approach for identifying the plant genetic variation associated with microbes in a community context. This review discusses early efforts on GWAS of the plant phyllosphere microbiome and the outlook for future studies based on human microbiome GWAS. A workflow for GWAS of the phyllosphere microbiome is then presented, with particular attention to how perspectives on the mechanisms, evolution and environmental dependence of plant–microbe interactions will influence the choice of traits to be mapped.     

Plant–plant interactions as a mechanism structuring plant diversity in a Mediterranean semi‐arid ecosystem

Plant–plant interactions are among the fundamental processes that shape structure and functioning of arid and semi‐arid plant communities. Despite the large amount of studies that have assessed the relationship between plant–plant interactions (i.e., facilitation and competition) and diversity, often researchers forget a third kind of interaction, known as allelopathy. We examined the effect of plant–plant interactions of three dominant species: the perennial grass Lygeum spartum, the allelopathic dwarf shrub Artemisia herba‐alba, and the nurse shrub Salsola vermiculata, on plant diversity and species composition in a semi‐arid ecosystem in NE Spain. Specifically, we quantified the interaction outcome (IO) based on species co‐occurrence, we analyzed diversity by calculation of the individual species–area relationship (ISAR), and compositional changes by calculation of the Chao‐Jaccard similarity index. We found that S. vermiculata had more positive IO values than L. spartum, and A. herba‐alba had values between them. Lygeum spartum and A. herba‐alba acted as diversity repellers, whereas S. vermiculata acted as a diversity accumulator. As aridity increased, A. herba‐alba transitioned from diversity repeller to neutral and S. vermiculata transitioned from neutral to diversity accumulator, while L. spartum remained as diversity repeller. Artemisia herba‐alba had more perennial grass species in its local neighborhood than expected by the null model, suggesting some tolerance of this group to its “chemical neighbor”. Consequently, species that coexist with A. herba‐alba were very similar among different A. herba‐alba individuals. Our findings highlight the role of the nurse shrub S. vermiculata as ecosystem engineer, creating and maintaining patches of diversity, as well as the complex mechanism that an allelopathic plant may have on diversity and species assemblage. Further research is needed to determine the relative importance of allelopathy and competition in the overall interference of allelopathic plants.     

Migration highways and migration barriers created by host–parasite interactions

Co‐evolving parasites may play a key role in host migration and population structure. Using co‐evolving bacteria and viruses, we test general hypotheses as to how co‐evolving parasites affect the success of passive host migration between habitats that can support different intensities of host–parasite interactions. First, we show that parasites aid migration from areas of intense to weak co‐evolutionary interactions and impede migration in the opposite direction, as a result of intraspecific apparent competition mediated via parasites. Second, when habitats show qualitative difference such that some environments support parasite persistence while others do not, different population regulation forces (either parasitism or competitive exclusion) will reduce the success of migration in both directions. Our study shows that co‐evolution with parasites can predictably homogenises or isolates host populations, depending on heterogeneity of abiotic conditions, with the second scenario constituting a novel type of ‘isolation by adaptation’.     

Early host–microbe interaction in a peri‐implant oral mucosa‐biofilm model

The host‐microbe relationship is pivotal for oral health as well as for peri‐implant diseases. Peri‐implant mucosa and commensal biofilm play important roles in the maintenance of host‐microbe homeostasis, but little is known about how they interact. We have therefore investigated the early host‐microbe interaction between commensal multispecies biofilm (Streptococcus oralis, Actinomyces naeslundii, Veillonella dispar, Porphyromonas gingivalis) and organotypic peri‐implant mucosa using our three‐dimensional model. After 24 hr, biofilms induced weak inflammatory reaction in the peri‐implant mucosa by upregulation of five genes related to immune response and increased secretion of IL‐6 and CCL20. Biofilm volume was reduced which might be explained by secretion of β‐Defensins‐1, ‐2, and CCL20. The specific tissue reaction without intrinsic overreaction might contribute to intact mucosa. Thus, a relationship similar to homeostasis and oral health was established within the first 24 hr. In contrast, the mucosa was damaged and the bacterial distribution was altered after 48 hr. These were accompanied by an enhanced immune response with upregulation of additional inflammatory‐related genes and increased cytokine secretion. Thus, the homeostasis‐like relationship was disrupted. Such profound knowledge of the host‐microbe interaction at the peri‐implant site may provide the basis to improve strategies for prevention and therapy of peri‐implant diseases.     

Effects of human–livestock–wildlife interactions on habitat in an eastern Kenya rangeland

Human–livestock–wildlife interactions have increased in Kenyan rangelands in recent years, but few attempts have been made to evaluate their impact on the rangeland habitat. This study identified drivers of increased human–livestock–wildlife interactions in the Meru Conservation Area between 1980 and 2000 and their effects on the vegetation community structure. The drivers were habitat fragmentation, decline in pastoral grazing range, loss of wildlife dispersal areas and increase in livestock population density. Agricultural encroachment increased by over 76% in the western zone adjoining Nyambene ranges and the southern Tharaka area, substantially reducing the pastoral grazing range and wildlife dispersal areas. Livestock population increased by 41%, subjecting areas left for pastoral grazing in the northern dispersal area to prolonged heavy grazing that gave woody plant species a competitive edge over herbaceous life‐forms. Consequently, open wooded grassland, which was the dominant vegetation community in 1980, decreased by c. 40% as bushland vegetation increased by 42%. A substantial proportion of agro pastoralists were encountered around Kinna and Rapsu, areas that were predominantly occupied by pastoralists three decades ago, indicating a possible shift in land use in order to spread risks associated with habitat alterations.     

Reevaluating the conceptual framework for applied research on host‐plant resistance

Applied research on host‐plant resistance to arthropod pests has been guided over the past 60 years by a framework originally developed by Reginald Painter in his 1951 book, Insect Resistance in Crop Plants. Painter divided the “phenomena” of resistance into three “mechanisms,” nonpreference (later renamed antixenosis), antibiosis, and tolerance. The weaknesses of this framework are discussed. In particular, this trichotomous framework does not encompass all known mechanisms of resistance, and the antixenosis and antibiosis categories are ambiguous and inseparable in practice. These features have perhaps led to a simplistic approach to understanding arthropod resistance in crop plants. A dichotomous scheme is proposed as a replacement, with a major division between resistance (plant traits that limit injury to the plant) and tolerance (plant traits that reduce amount of yield loss per unit injury), and the resistance category subdivided into constitutive/inducible and direct/indirect subcategories. The most important benefits of adopting this dichotomous scheme are to more closely align the basic and applied literatures on plant resistance and to encourage a more mechanistic approach to studying plant resistance in crop plants. A more mechanistic approach will be needed to develop novel approaches for integrating plant resistance into pest management programs.     

Evolution of spatially structured host–parasite interactions

Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host–parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life‐history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host–parasite life cycle and on which life‐history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host–parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.     

Influence of presence and spatial arrangement of belowground insects on host‐plant selection of aboveground insects: a field study

Abstract 1. Several studies have shown that above‐ and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host‐plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root‐feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar‐feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root‐feeding insect, naturally colonising populations of foliar‐feeding insects were monitored over the course of a summer season. 3. Groups of root‐infested and root‐uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root‐infested and the root‐uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root‐uninfested (control) than on root‐infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host‐plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root‐feeding insects can affect feeding and oviposition preferences of foliar‐feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root‐feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root‐feeding insects.     

Genetics of host–parasite interactions: towards a comprehensive dissection of Drosophila resistance to viral infection

One of the major challenges in evolutionary biology is to unravel the genetic basis of adaptation. This issue has been gaining momentum in recent years with the accelerated development of novel genetic and genomic techniques and resources. In this issue of Molecular Ecology, Cogni et al. (2016) address the genetic basis of resistance to two viruses in Drosophila melanogaster using a panel of recombinant inbred lines with unprecedented resolution allowing detection of rare alleles and/or alleles of small effect. The study confirms the role of previously identified genes of major effect and adds novel regions with minor effect to the genetic basis of Drosophila resistance to the Drosophila C virus or the sigma virus. Additional analyses reveal the absence of cross‐resistance and of epistasis between the various genomic regions. This detailed information on the genetic architecture of host resistance constitutes an important step towards the understanding of both the physiology of antiviral immunity and the evolution of host–parasite interactions.     

Microfluidic synthesis of composite cross‐gradient materials for investigating cell–biomaterial interactions

Combinatorial material synthesis is a powerful approach for creating composite material libraries for the high‐throughput screening of cell–material interactions. Although current combinatorial screening platforms have been tremendously successful in identifying target (termed “hit”) materials from composite material libraries, new material synthesis approaches are needed to further optimize the concentrations and blending ratios of the component materials. Here we employed a microfluidic platform to rapidly synthesize composite materials containing cross‐gradients of gelatin and chitosan for investigating cell–biomaterial interactions. The microfluidic synthesis of the cross‐gradient was optimized experimentally and theoretically to produce quantitatively controllable variations in the concentrations and blending ratios of the two components. The anisotropic chemical compositions of the gelatin/chitosan cross‐gradients were characterized by Fourier transform infrared spectrometry and X‐ray photoelectron spectrometry. The three‐dimensional (3D) porous gelatin/chitosan cross‐gradient materials were shown to regulate the cellular morphology and proliferation of smooth muscle cells (SMCs) in a gradient‐dependent manner. We envision that our microfluidic cross‐gradient platform may accelerate the material development processes involved in a wide range of biomedical applications. Biotechnol. Bioeng. 2011; 108:175–185. © 2010 Wiley Periodicals, Inc.     

Variation in the guild composition of herbivorous insect assemblages among co‐occurring plant species

Variation in plant traits among plant species may promote the development of a characteristic functional assemblage of insect herbivores associated with each plant species. However, only a small number of studies have detailed the representation of several herbivore guilds among co‐occurring plant species to determine whether the functional structure of herbivorous insect assemblages varies widely and consistently among plant species. The present study provides one of the few published data sets reporting on the density of several guilds of insect herbivores among numerous plant species. Variation in guild associations with plant phenology and season are also described. Insect herbivores were divided into 10 guilds, and the representation of these guilds was examined for 18 co‐occurring plant species. Guild densities and assemblage composition varied significantly among plant species, even when variation over time was taken into account. Variation in guild densities and assemblage composition were not strongly related to the taxonomic relationships of the plants. The highest densities of several guilds occurred in spring and summer, although other guilds were not strongly seasonal. Certain guilds were strongly associated with the presence of new leaves, whereas other guilds appeared to prefer mature leaves. This resulted in assemblage differences between samples containing new and mature leaves and samples containing mature leaves only. Even though the timing and duration of leaf and flower production varied among plant species, this did not explain all variation in guild densities among plant species. It is suggested that additional factors, including plant traits, are contributing to the wide and consistent variation in herbivore assemblage composition among plant species.     

Cation–π, amino–π, π–π, and H‐bond interactions stabilize antigen–antibody interfaces

The identification of immunogenic regions on the surface of antigens, which are able to stimulate an immune response, is a major challenge for the design of new vaccines. Computational immunology aims at predicting such regions—in particular B‐cell epitopes—but is far from being reliably applicable on a large scale. To gain understanding into the factors that contribute to the antigen–antibody affinity and specificity, we perform a detailed analysis of the amino acid composition and secondary structure of antigen and antibody surfaces, and of the interactions that stabilize the complexes, in comparison with the composition and interactions observed in other heterodimeric protein interfaces. We make a distinction between linear and conformational B‐cell epitopes, according to whether they consist of successive residues along the polypeptide chain or not. The antigen–antibody interfaces were shown to differ from other protein–protein interfaces by their smaller size, their secondary structure with less helices and more loops, and the interactions that stabilize them: more H‐bond, cation–π, amino–π, and π–π interactions, and less hydrophobic packing; linear and conformational epitopes can clearly be distinguished. Often, chains of successive interactions, called cation/amino–π and π–π chains, are formed. The amino acid composition differs significantly between the interfaces: antigen–antibody interfaces are less aliphatic and more charged, polar and aromatic than other heterodimeric protein interfaces. Moreover, paratopes and epitopes—albeit to a lesser extent—have amino acid compositions that are distinct from general protein surfaces. This specificity holds promise for improving B‐cell epitope prediction. Proteins 2014; 82:1734–1746. © 2014 Wiley Periodicals, Inc.     

Multi‐mode fluctuating selection in host–parasite coevolution

Understanding fluctuating selection is important for our understanding of patterns of spatial and temporal diversity in nature. Host–parasite theory has classically assumed fluctuations either occur between highly specific genotypes (matching allele: MA) or from specialism to generalism (gene‐for‐gene: GFG). However, while MA can only generate one mode of fluctuating selection, we show that GFG can in fact produce both rapid ‘within‐range’ fluctuations (among genotypes with identical levels of investment but which specialise on different subsets of the population) and slower cycling ‘between ranges’ (different levels of investment), emphasising that MA is a subset of GFG. Our findings closely match empirical observations, although sampling rates need to be high to detect these novel dynamics empirically. Within‐range cycling is an overlooked process by which fluctuating selection can occur in nature, suggesting that fluctuating selection may be a more common and important process than previously thought in generating and maintaining diversity.     

Mechanisms structuring host–parasitoid networks in a global warming context: a review

1. In natural communities, multiple host and parasitoid species are linked to form complex networks of trophic and non‐trophic interactions. Understanding how these networks will respond to global warming is of wide relevance for agriculture and conservation. 2. This study synthesises the emerging evidence surrounding host–parasitoid networks in the context of global warming. The suite of direct and indirect interaction types within host–parasitoid networks is summarised, as well as their sensitivity to temperature changes. The study also compiles and reviews studies investigating the responses of whole host–parasitoid networks to increasing temperatures or proxy variables. The findings reveal there is limited evidence overall for the prediction that parasitism will be reduced under global warming: approximately equal numbers of studies show elevated and reduced parasitism. 3. Increasingly, endosymbiotic bacteria are recognised as influential mediators of host–parasitoid interactions. These endosymbionts can change how individual species respond to global warming, and their effects can cascade to affect whole host–parasitoid networks. The evidence that symbiotic bacteria are likely to affect the response of host–parasitoid networks to global warming is reviewed. Symbionts can protect hosts from their parasitoids or influence thermal tolerance of their host species. Furthermore, the symbionts themselves can be impacted by global warming. 4. Finally, the study considers the most promising avenues for future research into the mechanisms structuring host–parasitoid networks in the context of global warming. Alongside the increasing availability of modern molecular methods to document the structure of real, species‐rich host–parasitoid networks, the study highlights the utility of manipulative experiments and mathematical models.     

Laying the groundwork for growth: Cell–cell and cell–ECM interactions in cardiovascular development

Cardiac development is reliant upon the spatial and temporal regulation of both genetic and chemical signals. Central to the communication of these signals are direct interactions between cells and their surrounding environment. The extracellular matrix (ECM) plays an integral role in cell communication and tissue growth throughout development by providing both structural support and chemical signaling factors. The present review discusses elements of cell–cell and cell–ECM interactions involved in cardiogenesis, and how disruption of these interactions can result in numerous heart defects. Examining the relationships between cells and their immediate environment has implications for novel and existing therapeutic strategies to combating congenital disorders. Birth Defects Research (Part C) 90:1–7, 2010. © 2010 Wiley‐Liss, Inc.