Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae

The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host–plant associations, uncovering the widespread co‐option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.

A high-quality functional genome assembly of Delia radicum L. (Diptera: Anthomiidae) annotated from egg to adult

Belowground herbivores are overseen and underestimated, even though they can cause significant economic losses in agriculture. The cabbage root fly Delia radicum (Anthomyiidae) is a common pest in Brassica species, including agriculturally important crops, such as oil seed rape. The damage is caused by the larvae, which feed specifically on the taproots of Brassica plants until they pupate. The adults are aboveground-living generalists feeding on pollen and nectar. Female flies are attracted by chemical cues in Brassica plants for oviposition. An assembled and annotated genome can elucidate which genetic mechanisms underlie the adaptation of D. radicum to its host plants and their specific chemical defenses, in particular isothiocyanates. Therefore, we assembled, annotated and analyzed the D. radicum genome using a combination of different Next Generation Sequencing and bioinformatic approaches. We assembled a chromosome-level D. radicum genome using PacBio and Hi-C Illumina sequence data. Combining Canu and 3D-DNA genome assembler, we constructed a 1.3 Gbp genome with an N50 of 242 Mbp and 6 pseudo-chromosomes. To annotate the assembled D. radicum genome, we combined homology-, transcriptome- and ab initio-prediction approaches. In total, we annotated 13,618 genes that were predicted by at least two approaches. We analyzed egg, larval, pupal and adult transcriptomes in relation to life-stage specific molecular functions. This high-quality annotated genome of D. radicum is a first step to understanding the genetic mechanisms underlying host plant adaptation. As such, it will be an important resource to find novel and sustainable approaches to reduce crop losses to these pests.

Comparative transcriptome analysis of the newly discovered insect vector of the pine wood nematode in China, revealing putative genes related to host plant adaptation

Background In many insect species, the larvae/nymphs are unable to disperse far from the oviposition site selected by adults. The Sakhalin pine sawyer Monochamus saltuarius (Gebler) is the newly discovered insect vector of the pine wood nematode (Bursaphelenchus xylophilus) in China. Adult M. saltuarius prefers to oviposit on the host plant Pinus koraiensis, rather than P. tabuliformis. However, the genetic basis of adaptation of the larvae of M. saltuarius with weaken dispersal ability to host environments selected by the adult is not well understood. Results In this study, the free amino and fatty acid composition and content of the host plants of M. saltuarius larvae, i.e., P. koraiensis and P. tabuliformis were investigated. Compared with P. koraiensis, P. tabuliformis had a substantially higher content of various free amino acids, while the opposite trend was detected for fatty acid content. The transcriptional profiles of larval populations feeding on P. koraiensis and P. tabuliformis were compared using PacBio Sequel II sequencing combined with Illumina sequencing. The results showed that genes relating to digestion, fatty acid synthesis, detoxification, oxidation-reduction, and stress response, as well as nutrients and energy sensing ability, were differentially expressed, possibly reflecting adaptive changes of M. saltuarius in response to different host diets. Additionally, genes coding for cuticle structure were differentially expressed, indicating that cuticle may be a potential target for plant defense. Differential regulation of genes related to the antibacterial and immune response were also observed, suggesting that larvae of M. saltuarius may have evolved adaptations to cope with bacterial challenges in their host environments. Conclusions The present study provides comprehensive transcriptome resource of M. saltuarius relating to host plant adaptation. Results from this study help to illustrate the fundamental relationship between transcriptional plasticity and adaptation mechanisms of insect herbivores to host plants.

Plant pathogen mediates rapid adaptation of insect to new host plant

The cotton-melon aphid, Aphis gossypii Glover, an extremely polyphagous pest insect, comprises of sympatric populations specialized on deferent host plants. The life history of A. gossypii infesting cucurbit crops remains elusive because oviparous aphids from overwintering hosts (often hibiscus) cannot colonize cucurbit crops. We verified that the hibiscus-specialized lineage (HI) suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs when transferred to fresh cucumber because the HI lineage was unable to ingest phloem sap from fresh cucumber. However, the HI lineage ingested phloem sap successfully when cucumber leaves were pre-infected with Pseudoperonospora cubensis, a biotrophic phytopathogen, accompanied by significant fitness improvement. More surprisingly, the HI lineage with feeding experience on pre-infected cucumber for two generations performed as well as the cucumber-specialized lineage (CU) did on fresh cucumber, and inflicted typical damage symptom to healthy cucumber plant. This phytopathogen mediated host plant adaptation may be widespread in polyphagous aphids.

Adaptation by copy number variation increases insecticide resistance in the fall armyworm

Understanding the genetic basis of insecticide resistance is a key topic in agricultural ecology. The adaptive evolution of multi-copy detoxification genes has been interpreted as a cause of insecticide resistance, yet the same pattern can also be generated by the adaptation to host-plant defense toxins. In this study, we tested in the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), if adaptation by copy number variation caused insecticide resistance in two geographically distinct populations with different levels of resistance and the two host-plant strains. We observed a significant allelic differentiation of genomic copy number variations between the two geographic populations, but not between host-plant strains. A locus with positively selected copy number variation included a CYP gene cluster. Toxicological tests supported a central role for CYP enzymes in deltamethrin resistance. Our results indicate that copy number variation of detoxification genes might be responsible for insecticide resistance in fall armyworm and that evolutionary forces causing insecticide resistance could be independent of host-plant adaptation.

Highly conserved genes expressed in aphid saliva are candidates for host plant adaptation in Aphis gossypii

BackgroundAphids are major crop pests, most species attacking crops specialize on a narrow range of plant species from a single family. By contrast, Aphis gossypii is a highly polyphagous species, for which host races specializing on particular crops have been clearly described. Salivary components, which aphids inject into the phloem via their stylets, play a key role in establishing compatible interactions between plants and aphids, and are probably involved in specialization.ResultsWe used the extensive resources available for Myzus persicae and Acyrthosiphon pisum to identify putative salivary proteins expressed in Aphis gossypii, despite the lack of genomic resources for this species. In silico, we identified 51 putative salivary proteins; we focused on 17 genes with orthologs in at least one aphid species, assuming that some of the conserved genes expressed in salivary glands are involved in host specialization. We amplified and sequenced 10 coding sequences in full, from 17 clones of Aphis gossypii specialising on plants from Malvaceae, Cucurbitaceae or Solanaceae. We reconstructed the phylogenetic tree for these genes, on which we identified a clade corresponding to all clones specializing on cucurbits. Three of these genes were under positive selection.ConclusionsFull adaptation to a particular host plant may require a combination of alleles at quantitative trait loci in aphids. The three genes we identified could potentially be part of a cocktail of effectors manipulating the immune system of cucurbits and therefore responsible for A. gossypii specialization on that plant family.

Inside out: microbiota dynamics during host-plant adaptation of whiteflies

While most insect herbivores are selective feeders, a small proportion of them feed on a wide range of plants. This polyphagous habit requires overcoming a remarkable array of defenses, which often necessitates an adaptation period. Efforts for understanding the mechanisms involved mostly focus on the insect’s phenotypic plasticity. Here, we hypothesized that the adaptation process might partially rely on transient associations with bacteria. To test this, we followed in a field-like experiment, the adaptation process of Bemisia tabaci, a generalist sap feeder, to pepper (a less-suitable host), after switching from watermelon (a suitable host). Amplicon sequencing of 16S rRNA transcripts from hundreds of dissected guts revealed the presence of active “core” and “transient” bacterial communities, dominated by the phyla Proteobacteria, Actinobacteria, and Firmicutes, and increasing differences between populations grown on watermelon and pepper. Insects grown on pepper for over two generations presented a significant increase in specific genera, mainly Mycobacterium, with a predicted enrichment in degradative pathways of xenobiotics and secondary metabolites. This result correlated with a significant increase in the insect’s survival on pepper. Taken together, our findings suggest that gut-associated bacteria can provide an additional flexible metabolic “tool-box” to generalist sap feeders for facilitating a quick host switching process.