The Host-Plant Origin Affects the Morphological Traits and the Reproductive Behavior of the Aphid Parasitoid Aphelinus mali

Diversifying agroecosystems through habitat management inside or outside production fields can provide alternative hosts and/or prey for natural enemies. In semi-natural habitats, parasitoids may find alternative host-plant complexes (HPC) that could allow their development when pest hosts are scarce in the field. However, morphological and physiological differences between alternative and targeted HPCs could affect the preference and fitness of the parasitoids, possibly altering their efficacy in regulating pests. In the present study, we examined two Aphelinus mali parasitoid populations developing on Eriosoma lanigerum from two host plants (Malus domestica-apple trees and Pyracantha coccinea). We hypothesized that A. mali from both HPCs will show different life history traits and behaviors because primary and alternative host-plants are known to induce variations in parasitoid biological performance. Our findings indicate that A. mali originating from E. lanigerum on P. coccinea parasitized more aphids and are smaller than those originating from E. lanigerum on apple. Furthermore, these parasitoids did not significantly vary their ability to attack and oviposit apple E. lanigerum, suggesting that P. coccinea could function as a suitable banker plant for A. mali. We discuss the potential use of P. coccinea in conservation biological control of E. lanigerum in apple orchards.

Chromosome-level genome assembly of the horned-gall aphid, Schlechtendalia chinensis (Hemiptera: Aphididae: Erisomatinae)

The horned gall aphid Schlechtendalia chinensis, is an economically important insect that induces galls valuable for medicinal and chemical industries. S. chinensis manipulates its host plant to form well-organized horned galls during feeding. So far, more than twenty aphid genomes have been reported; however, all of those are derived from free-living aphids. Here we generated a high-quality genome assembly of S. chinensis, representing the first genome sequence of a galling aphid. The final genome assembly was 280.43 Mb, with 97% of the assembled sequences anchored into thirteen chromosomes. S. chinensis presents the smallest aphid genome size among available aphid genomes to date. The contig and scaffold N50 values were 3.39 Mb and 20.58 Mb, respectively. The assembly included 96.4% of conserved arthropod and 97.8% of conserved Hemiptera single-copy orthologous genes based on BUSCO analysis. A total of 13,437 protein-coding genes were predicted. Phylogenomic analysis showed that S. chinensis formed a single clade between the Eriosoma lanigerum clade and the Aphidini+Macrosiphini aphid clades. In addition, salivary proteins were found to be differentially expressed when S. chinensis underwent host alternation, indicating their potential roles in gall formation and plant defense suppression. A total of 36 cytochrome P450 genes were identified in S. chinensis, considerably fewer compared to other aphids, probably due to its small host plant range. The high-quality S. chinensis genome assembly and annotation provide an essential genetic background for future studies to reveal the mechanism of gall formation and to explore the interaction between aphids and their host plants.

EPG analysis of stylet penetration preference of woolly apple aphid on different parts of apple trees

Woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann), is an important global pest that feeds on Malus species. We studied the feeding preference of WAA on apple trees in the field for two consecutive years and in the laboratory we used electronic penetration graphs (EPG) to record the stylet penetration behavior of WAA on different parts of apple trees. We found that in the field WAA fed primarily on twigs and branches, not on leaves and fruits. Six EPG waveforms were produced during WAA probing on shoots, trunks and leaves of apple trees, including the non-penetration wave (np), the stylet pathway phase wave (C), the intracellular feeding wave (pd), the xylem feeding wave (G), waves indicative of release of saliva into the phloem (E1), and a wave indicative of ingestion from phloem (E2). In the laboratory, aphids only successfully fed on shoots, trunks and leaves, not on fruits. The EPG parameters on the phloem of shoots were significantly higher than those on trunks, indicating WAA prefer to feed on shoots. These laboratory findings explain the relative field feeding preference of WAA on different parts of apple trees, which occurs primarily on branches, barks, and young twigs in orchards, especially on young twigs.

Chromosome-level genome assembly of the horned-gall aphid, Schlechtendalia chinensis (Hemiptera: Aphididae: Erisomatinae)

The horned gall aphid Schlechtendalia chinensis, is an economically important insect that induces galls valuable for medicinal and chemical industries. S. chinensis manipulates its host plant to form well-organized horned galls during feeding. So far, more than twenty aphid genomes have been reported; however, all of those are derived from free-living aphids. Here we generated a high-quality genome assembly of S. chinensis, representing the first genome sequence of a galling aphid. The final genome assembly was 280.43 Mb, with 97% of the assembled sequences anchored into thirteen chromosomes. S. chinensis presents the smallest aphid genome size among available aphid genomes to date. The contig and scaffold N50 values were 3.39 Mb and 20.58 Mb, respectively. The assembly included 96.4% of conserved arthropod and 97.8% of conserved Hemiptera single-copy orthologous genes based on BUSCO analysis. A total of 13,437 protein-coding genes were predicted. Phylogenomic analysis showed that S. chinensis formed a single clade between the Eriosoma lanigerum clade and the Aphidini+Macrosiphini aphid clades. In addition, salivary proteins were found to be differentially expressed when S. chinensis underwent host alternation, indicating their potential roles in gall formation and plant defense suppression. A total of 36 cytochrome P450 genes were identified in S. chinensis, considerably fewer compared to other aphids, probably due to its small host plant range. The high-quality S. chinensis genome assembly and annotation provide an essential genetic background for future studies to reveal the mechanism of gall formation and to explore the interaction between aphids and their host plants.

Resistance performance of four principal apple cultivars to woolly apple aphid, Eriosoma lanigerum (Hemiptera: Pemphigidae), by simulated seasonal temperature in northern China

Woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann) (Hemiptera: Pemphigidae), is a worldwide quarantine pest of apples. Understanding the resistance mechanism of various cultivars to WAA is important for the selection for durable resistance. Few studies have examined the resistance of different apple cultivars to WAA in China; among common varieties produced in China, Red Fuji is highly sensitive to WAA. In this study, the resistance to WAA of Red Fuji and three other common cultivars—Starkrimson, Jonagold, and Ralls Genet—was assessed based on the developmental and reproductive biological characteristics of aphids, assessed under four fixed temperatures: 20, 25, 30, and 35 ℃. We found the optimal temperature for WAA growth and reproduction to be 20–25 ℃, at which temperature, aphids on Red Fuji showed the highest rate of reproduction, the highest number of colonies, and the greatest area covered by aphid colonies among the four cultivars. These attributes of WAA were significantly higher at 20–25 ℃ than at 30 ℃. On Red Fuji, the most favorable variety, WAA showed its highest net reproductive rate (127.3 ± 13.3), intrinsic growth rate (0.30 ± 0.01), highest growth rate of the colony area (1.35 ± 0.02), and the lowest average generation time (16.1 ± 0.8 day) at 25 ℃. The aphids inoculated onto the four tested cultivars all died within 1 week at 35 ℃. Overall, Red Fuji was highly susceptible, while Starkrimson, Jonagold, and Ralls Genet were partially resistant.

Biological properties and influencing factors of woolly apple aphid (Eriosoma lanigerum Hausm) in the condition of orchard agrobiocenosis

This article provides information on the influence of biotic and abiotic factors on the development of the population of orchard agrobiocenosis of woolly apple aphid (Eriosoma lanigerum Hausm), the main sucking pest of seed orchards.

A chromosome-level genome assembly of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae)

ABSTRACTWoolly apple aphid (WAA, Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), is a major pest of apple trees (Malus domestica, order Rosales) and is critical to the economics of the apple industry in most parts of the world. Here, we generated a chromosome-level genome assembly of WAA – representing the first genome sequence from the aphid subfamily Eriosomatinae – using a combination of 10X Genomics linked-reads and in vivo Hi-C data. The final genome assembly is 327 Mb, with 91% of the assembled sequences anchored into six chromosomes. The contig and scaffold N50 values are 158 kb and 71 Mb, respectively, and we predicted a total of 28,186 protein-coding genes. The assembly is highly complete, including 97% of conserved arthropod single-copy orthologues based on BUSCO analysis. Phylogenomic analysis of WAA and nine previously published aphid genomes, spanning four aphid tribes and three subfamilies, reveals that the tribe Eriosomatini (represented by WAA) is recovered as a sister group to Aphidini + Macrosiphini (subfamily Aphidinae). We identified syntenic blocks of genes between our WAA assembly and the genomes of other aphid species and find that two WAA chromosomes (El5 and El6) map to the conserved Macrosiphini and Aphidini X chromosome. Our high-quality WAA genome assembly and annotation provides a valuable resource for research in a broad range of areas such as comparative and population genomics, insect-plant interactions and pest resistance management.

Comparative Analysis of Stylet Penetration Behaviors of Eriosoma lanigerum (Hemiptera: Aphididae) on Main Apple Cultivars in China

The preference and behavioral mechanism of the feeding behavior of the woolly apple aphid, Eriosoma lanigerum (Hausmann), on Chinese apple cultivars was investigated using the electrical penetration graph (EPG) technique. Feeding of adult aphids was assessed for the four main cultivars of apple in China (Red Fuji, Ralls Genet, Starkrimson, and Jonagold) over an 8-h monitoring period, what that of fourth-instar nymphs was assessed for 8 h on Jonagold only. EPG waveforms representing the details of probing behaviors, parameters were measured for analysis. We found that at the nonphloem phase, the total duration of the nonpenetration (np) waveform and the total duration of the stylet pathway phase (the ‘C wave’) on Ralls Genet and Starkrimson were significantly longer than on Red Fuji. In addition, the phloem-feeding phase, the total duration of ‘release of saliva into the phloem’, (the E1 waveform) was significantly longer on Ralls Genet and Jonagold than on Red Fuji. The total duration of the ‘ingestion from sieve cells’ phase (the E2 waveform) on Red Fuji, meanwhile, was significantly longer than on Ralls Genet or Starkrimson. At the same time, when combined with EPG parameters, Red Fuji was found to have no obvious resistance to woolly apple aphid and to be a susceptible cultivar. This experiment also recorded the feeding waveform of fourth-instar aphid nymphs. Based on the phloem and nonphloem parameters recorded in this study, it was inferred that adult aphids are more likely than nymphs to feed on apple trees.