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ABSTRACT It is often taken for granted that all animals host and depend upon a microbiome, yet this has only been shown for a small proportion of species. We propose that animals span a continuum of reliance on microbial symbionts. At one end are the famously symbiont-dependent species such as aphids, humans, corals and cows, in which microbes are abundant and important to host fitness. In the middle are species that may tolerate some microbial colonization but are only minimally or facultatively dependent. At the other end are species that lack beneficial symbionts altogether. While their existence may seem improbable, animals are capable of limiting microbial growth in and on their bodies, and a microbially independent lifestyle may be favored by selection under some circumstances. There is already evidence for several ‘microbiome-free’ lineages that represent distantly related branches in the animal phylogeny. We discuss why these animals have received such little attention, highlighting the potential for contaminants, transients, and parasites to masquerade as beneficial symbionts. We also suggest ways to explore microbiomes that address the limitations of DNA sequencing. We call for further research on microbiome-free taxa to provide a more complete understanding of the ecology and evolution of macrobe-microbe interactions. Contrary to a prevailing paradigm, some animals do not host nor rely on a microbiome.

Aphids transmit viruses and are destructive crop pests 1 . Plants that have been attacked by aphids release volatile compounds to elicit airborne defence (AD) in neighbouring plants 2 – 5 . However, the mechanism underlying AD is unclear. Here we reveal that methyl-salicylate (MeSA), salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2 and salicylic acid-carboxylmethyltransferase-1 (SAMT1) form a signalling circuit to mediate AD against aphids and viruses. Airborne MeSA is perceived and converted into salicylic acid by SABP2 in neighbouring plants. Salicylic acid then causes a signal transduction cascade to activate the NAC2–SAMT1 module for MeSA biosynthesis to induce plant anti-aphid immunity and reduce virus transmission. To counteract this, some aphid-transmitted viruses encode helicase-containing proteins to suppress AD by interacting with NAC2 to subcellularly relocalize and destabilize NAC2. As a consequence, plants become less repellent to aphids, and more suitable for aphid survival, infestation and viral transmission. Our findings uncover the mechanistic basis of AD and an aphid–virus co-evolutionary mutualism, demonstrating AD as a potential bioinspired strategy to control aphids and viruses. Aphid-transmitted viruses encode proteins that suppress the plant airborne defence response—which is triggered by volatile chemicals released by neighbouring plants after aphid attack—and the plants consequently become less repellent to aphids and more suitable for aphid survival, infestation and viral transmission.

1. Landscape-level crop diversification is a promising tool for ecological intensification, whereby biodiversity and ecosystem services are enhanced, and pesticide applications reduced. Yet evidence for the effects of crop diversity at multiple scales and in different landscape contexts is lacking. Here, we investigate the potential benefits and context dependencies of multiscale crop diversity on natural enemies and overall biological control in winter wheat. Simultaneously, we examine the mediating effects of bird predation on aphid regulation in this system. 2. Eighteen conventional winter wheat fields were selected along two independent gradients of crop diversity and semi-natural habitat cover (SNH). We assessed biological control using a natural enemy exclusion experiment (''Open Treatment,\" \"Bird Exclosure,\" \"Full Exclosure\"). Biological control, predator and parasitoid densities within cages were analysed as functions of landscape (crop diversity × SNH), bird predation (yes/no) and temporal change (three surveys) on six spatial scales (100-3,000 m). 3. Crop diversity rather than SNH enhanced aphid regulation in our study system. Biological control in fields with high landscape-level crop diversity was 8%-33% higher than in low-diversity landscapes, with main effects observed on scales <500 m. 4. Predator and parasitoid densities increased with crop diversity on small (100250 m) and large (2,000-3,000 m) spatial scales respectively. Nevertheless, our findings suggest that natural enemies other than birds, parasitoids and aerial arthropods facilitated biological control. 5. Synthesis and applications. Our study shows that landscape-level crop diversification can improve biological control in agroecosystems. Therefore, increased crop diversity could lower dependence on insecticides while enhancing yield stability through ecological intensification of farming. We also highlight the need to assess biological control rather than natural enemy abundances to avoid bias due to sampling artefacts or species interactions. Finally, simple measures of crop diversity (e.g. \"effective number of crop types\") help in science communication and the development of farm management guidelines.

Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding insects, and Buchnera aphidicola , a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host–symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host–pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphid– Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.

Potyviruses are the largest group of plant infecting RNA viruses that cause significant losses in a wide range of crops across the globe. The majority of viruses in the genus Potyvirus are transmitted by aphids in a non-persistent, non-circulative manner and have been extensively studied vis-à-vis their structure, taxonomy, evolution, diagnosis, transmission, and molecular interactions with hosts. This comprehensive review exclusively discusses potyviruses and their transmission by aphid vectors, specifically in the light of several virus, aphid and plant factors, and how their interplay influences potyviral binding in aphids, aphid behavior and fitness, host plant biochemistry, virus epidemics, and transmission bottlenecks. We present the heatmap of the global distribution of potyvirus species, variation in the potyviral coat protein gene, and top aphid vectors of potyviruses. Lastly, we examine how the fundamental understanding of these multi-partite interactions through multi-omics approaches is already contributing to, and can have future implications for, devising effective and sustainable management strategies against aphid-transmitted potyviruses to global agriculture.

The thermal tolerance of an organism limits its ecological and geographic ranges and is potentially affected by dependence on temperature-sensitive symbiotic partners. Aphid species vary widely in heat sensitivity, but almost all aphids are dependent on the nutrient-provisioning intracellular bacterium Buchnera, which has evolved with aphids for 100 million years and which has a reduced genome potentially limiting heat tolerance. We addressed whether heat sensitivity of Buchnera underlies variation in thermal tolerance among 5 aphid species. We measured how heat exposure of juvenile aphids affects later survival, maturation time, and fecundity. At one extreme, heat exposure of Aphis gossypii enhanced fecundity and had no effect on the Buchnera titer. In contrast, heat suppressed Buchnera populations in Aphis fabae, which suffered elevated mortality, delayed development and reduced fecundity. Likewise, in Acyrthosiphon kondoi and Acyrthosiphon pisum, heat caused rapid declines in Buchnera numbers, as well as reduced survivorship, development rate, and fecundity. Fecundity following heat exposure is severely decreased by a Buchnera mutation that suppresses the transcriptional response of a gene encoding a small heat shock protein. Similarly, absence of this Buchnera heat shock gene may explain the heat sensitivity of Ap. fabae. Fluorescent in situ hybridization revealed heat-induced deformation and shrinkage of bacteriocytes in heat-sensitive species but not in heat-tolerant species. Sensitive and tolerant species also differed in numbers and transcriptional responses of heat shock genes. These results show that shifts in Buchnera heat sensitivity contribute to host variation in heat tolerance.

1. Sown flower strips are increasingly implemented within agri-environment schemes (AES) to increase functional biodiversity and ecosystem services such as pollination or natural pest control, but their effectiveness in achieving these goals remains poorly studied. 2. We tested the performance of experimentally sown annual flower strips specifically designed to promote natural enemies of aphids and their pest control services (tailored flower strips) in adjacent potato crops (n = 8) compared with control fields (n = 10). Flower strips consisted of 11 plant species providing abundant floral and extra-floral resources. 3. The abundance of key natural enemies of aphids (hoverflies, lacewings and ladybirds) and hoverfly species richness was greatly enhanced in tailored flower strips compared with potato control strips. This resulted in an average increase in the number of eggs deposited by hoverflies and lacewings by 127% and 48%, respectively, and a reduction in the number of aphids by 75% in adjacent potato crops. 4. Synthesis and applications. We conclude that tailored flower strips can be an effective agrienvironmental measure to enhance natural enemies and aphid control in nearby crops. Indeed, tailored flower strips may help to reduce insecticide input in potato production as they significantly decrease the probability that action thresholds are reached. Promoting natural enemy abundance and diversity, as observed for hoverflies, may increase the stability of pest control and provide additional benefits to agro-ecosystems in terms of natural enemy conservation. We thus recommend establishing tailored flower strips as a promising management option to reconcile the objectives of ecological intensification and biodiversity conservation.

The first observation of alate gyne of Dolichoderusquadripunctatus (L.) visiting aphids is described. A gyne walked along a foraging trail to the aphid Panaphisjuglandis Goeze colony where it imbibed honeydew excreted on the leaf by the aphids, after which it returned to the trail. This recurred during two more days, always a single alate gyne at a time; hence the total number of gynes, one or more, remained open. The phenomenon, hitherto practically unknown in ants, is presented against the background of the biology of the species and discussed in the context of specific environmental circumstances and the colony dynamics.

• Entomopathogenic fungi (EPF) can display a plant-associated lifestyle as endophytes. Seed application of EPF can affect insect herbivory above ground, but the mechanisms behind this are not documented. • Here we applied three EPF isolates, Beauveria bassiana, Metarhizium brunneum and M. robertsii, as seed inoculation of wheat and bean, and evaluated the effects on population growth of aphids, Rhopalosiphum padi and Aphis fabae, respectively. In wheat and bean leaves, we quantified benzoxazinoids and flavonoids, respectively, in response to EPF inoculation and aphid infestation to elucidate the role of specific plant secondary metabolites (PSMs) in plant–fungus–herbivore interactions. • Inoculations of wheat and bean with M. robertsii and B. bassiana reduced aphid populations compared with control treatments, whereas M. brunneum unexpectedly increased the populations of both aphids. Concentrations of the majority of PSMs were differentially altered in EPF-treated plants infested with aphids. Changes in aphid numbers were associated with PSMs regulation rather than EPF endophytic colonisation capacity. • This study links the effects of EPF seed inoculations against aphids with unique PSM accumulation patterns in planta. The understanding of PSM regulation in tri-trophic interactions is important for the future development of EPF for pest management.

BACKGROUND: The prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Insect herbivores are no exception and the majority have evolved to colonise a small number of closely related host species. Remarkably, the green peach aphid, Myzus persicae, colonises plant species across 40 families and single M. persicae clonal lineages can colonise distantly related plants. This remarkable ability makes M. persicae a highly destructive pest of many important crop species. RESULTS: To investigate the exceptional phenotypic plasticity of M. persicae, we sequenced the M. persicae genome and assessed how one clonal lineage responds to host plant species of different families. We show that genetically identical individuals are able to colonise distantly related host species through the differential regulation of genes belonging to aphid-expanded gene families. Multigene clusters collectively upregulate in single aphids within two days upon host switch. Furthermore, we demonstrate the functional significance of this rapid transcriptional change using RNA interference (RNAi)-mediated knock-down of genes belonging to the cathepsin B gene family. Knock-down of cathepsin B genes reduced aphid fitness, but only on the host that induced upregulation of these genes. CONCLUSIONS: Previous research has focused on the role of genetic adaptation of parasites to their hosts. Here we show that the generalist aphid pest M. persicae is able to colonise diverse host plant species in the absence of genetic specialisation. This is achieved through rapid transcriptional plasticity of genes that have duplicated during aphid evolution.