2024-05-20 2024, Volume 31 Issue 5

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  • REVIEW
    Mauricio Roberto Vianna Sant’Anna , Adalberto Alves Pereira-Filho , Antonio Ferreira Mendes-Sousa , Naylene Carvalho Sales Silva , Nelder Figueiredo Gontijo , Marcos Horácio Pereira , Leonardo Barbosa Koerich , Grasielle Caldas D’Avila Pessoa , John Andersen , Ricardo Nascimento Araujo
    2024, 31(5): 1334-1352. https://doi.org/10.1111/1744-7917.13317

    In arthropods, hematophagy has arisen several times throughout evolution. This specialized feeding behavior offered a highly nutritious diet obtained during blood feeds. On the other hand, blood-sucking arthropods must overcome problems brought on by blood intake and digestion. Host blood complement acts on the bite site and is still active after ingestion, so complement activation is a potential threat to the host’s skin feeding environment and to the arthropod gut enterocytes. During evolution, blood-sucking arthropods have selected, either in their saliva or gut, anticomplement molecules that inactivate host blood complement. This review presents an overview of the complement system and discusses the arthropod’s salivary and gut anticomplement molecules studied to date, exploring their mechanism of action and other aspects related to the arthropod–host–pathogen interface. The possible therapeutic applications of arthropod’s anticomplement molecules are also discussed.

  • REVIEW
    Chenyu Qian , Chao Wen , Xiaoli Guo , Xinya Yang , Xiujun Wen , Tao Ma , Cai Wang
    2024, 31(5): 1353-1364. https://doi.org/10.1111/1744-7917.13312

    The gregarious lifestyle of lepidopteran larvae is diverse and shaped by a complex interplay of ecological and evolutionary factors. Our review showed that the larval-aggregation behavior has been reported in 23 lepidopteran families, indicating multiple evolution of this behavior. Some larvae live in sibling groups throughout all larval instars and even pupation stages, which may result from the kin-selection. In contrast, group fusion may occur among different sibling or foraging groups of larvae and form larger aggregates, and the gregariousness of these species might be driven by the group-selection. While group size and foraging patterns vary greatly across species, it is generally associated with improved larval survivorship and accelerated development. However, the advantages of group living, such as facilitating feeding activities, adjusting the temperature, and defending natural enemies, may diminish along with development, with strong intraspecific competition occurring at later instars, even when food is abundant. Therefore, the group sizes and fission–fusion dynamics of certain gregarious lepidopteran larvae may be a consequence of their cost–benefit balance depending on various biotic and abiotic factors. Trail and aggregation pheromones, silk trails, or body contact contribute to collective movement and group cohesion of gregarious lepidopteran larvae. However, frequent contact among group members may cause the horizontal transmission of pathogens and pesticides, which may bring an integrated pest management strategy controlling gregarious lepidopteran pests.

  • ORIGINAL ARTICLE
    Yansong Wang , Ping Gao , Wenquan Qin , Hongran Li , Jie Zheng , Ling Meng , Baoping Li
    2024, 31(5): 1365-1377. https://doi.org/10.1111/1744-7917.13310

    We attempt to determine the effect of the dietary switch from a native to non-native prey on the gut microbiota in the predaceous ladybird Harmonia axyridis larvae and adults and examine how the dietary effect may vary across generations. We fed H. axyridis with different diets, native aphid Megoura japonica (Matsumura) versus non-native mealybug Phenacoccus solenopsis (Tinsley), for 5 generations and sequenced microbes in the gut of the 3rd instar larvae and adults of the 1st, 3rd, and 5th generations. In addition, we identified microbes in M. japonica and P. solenopsis. The 2 prey species differed in microbial community as measured by abundances of prevalent microbial genera and diversity. In H. axyridis, abundances of some prevalent microbial genera differed between the 2 diets in the 1st and 3rd generations, but the difference disappeared in the 5th generation; this tendency is more obvious in adults than in larvae. Overall, gut microbial assemblages became gradually cohesive over generations. Microbial diversity differed between diets in the 1st and 3rd generations but became similar in the 5th generation. Major prevalent gut microbial genera are predicted to be associated with metabolic functions of H. axyridis and associated genera are more abundant for consuming the mealybug than the aphid. Our findings from this study suggest that the gut microbiota in H. axyridis is flexible in response to the dietary switch, but tends toward homogeneity in microbial composition over generations.

  • ORIGINAL ARTICLE
    Hui-Hua Cao , Wei-Wei Kong , Bing Ling , Zhi-Yi Wang , Ying Zhang , Zhe-Xiao Guo , Shi-Huo Liu , Jia-Ping Xu
    2024, 31(5): 1378-1396. https://doi.org/10.1111/1744-7917.13318

    MicroRNAs (miRNAs) are small non-coding RNAs that play pivotal roles in the host response to invading pathogens. Among these pathogens,Bombyx mori nucleopolyhedrovirus (BmNPV) is one of the main causes of substantial economic losses in sericulture, and there are relatively few studies on the specific functions of miRNAs in the B. mori–BmNPV interaction. Therefore, we conducted transcriptome sequencing to identify differentially expressed (DE) messenger RNAs (mRNAs) and miRNAs in the midgut of 2 B. mori strains (BmNPV-susceptible strain P50 and BmNPV-resistant strain A35) after BmNPV infection. Through correlation analysis of the miRNA and mRNA data, we identified a comprehensive set of 21 miRNAs and 37 predicted target mRNAs. Notably, miR-3351, which has high expression in A35, exhibited remarkable efficacy in suppressing BmNPV proliferation. Additionally, we confirmed that miR-3351 binds to the 3’untranslated region (3’UTR) of B. mori glutathione S-transferase epsilon 6 (BmGSTe6), resulting in its downregulation. Conversely,BmGSTe6 displayed an opposite expression pattern to miR-3351, effectively promoting BmNPV proliferation. Notably,BmGSTe6 levels were positively correlated with glutathione S-transferase activity, consequently influencing intracellular glutathione content in the infected samples. Furthermore, our investigation revealed the protective role of glutathione against BmNPV infection in BmN cells. In summary, miR-3351 modulates glutathione content by downregulating BmGSTe6 to inhibit BmNPV proliferation in B. mori. Our findings enriched the research on the role of B. mori miRNAs in the defense against BmNPV infection, and suggests that the antiviral molecule, glutathione, offers a novel perspective on preventing viral infection in sericulture.

  • ORIGINAL ARTICLE
    Yunlong Zou , Wentao Wu , Tianfu Luo , Yuxia Tang , Hai Hu , Aijun Ye , Lifeng Xu , Fangyin Dai , Xiaoling Tong
    2024, 31(5): 1397-1411. https://doi.org/10.1111/1744-7917.13354

    Feeding behavior is critical for insect survival and fitness. Most researchers have explored the molecular basis of feeding behaviors by identifying and elucidating the function of olfactory receptors (ORs) and gustatory receptors (GRs). Other types of genes, such as transcription factors, have rarely been investigated, and little is known about their potential roles. The silkworm (Bombyx mori) is a well-studied monophagic insect which primarily feeds on mulberry leaves, but the genetic basis of its monophagy is still not understood. In this report, we focused on a transcription factor encoded by the Zfh3 gene, which is highly expressed in the silkworm central and peripheral nervous systems, including brain, antenna, and maxilla. To investigate its function,Zfh3 was abrogated using clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR associated protein 9 (Cas9) mutagenesis. Since Zfh3 knockout homozygotes are not viable, we studied feeding behavior in heterozygotes, and found that disruption of Zfh3 affects both gustation and olfaction. Mutant larvae lose preference for mulberry leaves, acquire the ability to consume an expanded range of diets, and exhibit improved adaptation to the M0 artificial diet, which contains no mulberry leaves. These results provide the first demonstration that a transcription factor modulates feeding behaviors in an insect.

  • ORIGINAL ARTICLE
    Rong-Rong Yu , Jia-Qi Duan , Xiao-Ming Zhao , Mureed Abbas , Yu-Ping Zhang , Xue-Kai Shi , Nan Chen , Jian-Zhen Zhang
    2024, 31(5): 1412-1424. https://doi.org/10.1111/1744-7917.13313

    The foregut, located at the front of the digestive tract, serves a vital role in insects by storing and grinding food into small particles. The innermost layer of the foregut known as the chitinous intima, comes into direct contact with the food and acts as a protective barrier against abrasive particles. Knickkopf (Knk) is required for chitin organization in the chitinous exoskeleton, tracheae and wings. Despite its significance, little is known about the biological function of Knk in the foregut. In this study, we found that LmKnk was stably expressed in the foregut, and highly expressed before molting in Locusta migratoria. To ascertain the biological function of LmKnk in the foregut, we synthesized specific double-stranded LmKnk (dsLmKnk) and injected it into locusts. Our findings showed a significant decrease in the foregut size, along with reduced food intake and accumulation of residues in the foregut after dsLmKnk injection. Morphological observations revealed that newly formed intima became thinner and lacked chitin lamella. Furthermore, fluorescence immunohistochemistry revealed that LmKnk was located in the apical region of new intima and epithelial cells. Taken together, this study provides insights into the biological function of LmKnk in the foregut, and identifies the potential target gene for exploring biological pest management strategies.

  • ORIGINAL ARTICLE
    Xin Tang , Huawei Liu , Xin Wang , Li Chang , Qingsong Liu , Qingyou Xia , Ping Zhao
    2024, 31(5): 1425-1439. https://doi.org/10.1111/1744-7917.13314

    Insects produce silk to form cocoons, nests, and webs, which are important for their survival and reproduction. However, little is known about the molecular mechanism of silk protein synthesis at the translation level. The solute carrier family 7 (SLC7) genes are involved in activating the target of rapamycin complex 1 (TORC1) signaling pathway and protein translation process, but the physiological roles of SLC7 genes in silk-producing insects have not been reported. Here, we found that amino acid signaling regulates silk protein synthesis and larval development via the L-type amino acid transporter 1 (LAT1; also known as SLC7A5) in Bombyx mori. A total of 12 SLC7 homologs were identified in the silkworm genome, among which BmSLC7A5 was found to be a silk gland-enriched gene and may be involved in leucine transport. Bioinformatics analysis indicated that SLC7A5 displays high homology and a close phylogenetic relationship in silk-producing insects. Subsequently, we found that leucine treatment significantly increased silk protein synthesis by improving the transcription and protein levels of silk genes. Furthermore, systemic and silk gland-specific knockout of BmSLC7A5 led to decreased silk protein synthesis by inhibiting TORC1 signaling, and somatic mutation also resulted in arrested development from the 5th instar to the early pupal stage. Altogether, our study reveals that BmSLC7A5 is involved in regulating silk protein synthesis and larval development by affecting the TORC1 signaling pathway, which provides a new strategy and target for improving silk yield.

  • ORIGINAL ARTICLE
    Yanfei Chen , Jin Li , Kangkang Niu , Yuling Peng , Qisheng Song , Qili Feng
    2024, 31(5): 1440-1452. https://doi.org/10.1111/1744-7917.13334

    Advanced DNA structures, such as the G-quadruplex (G4) and the i-motif, are widely but not randomly present in the genomes of many organisms. A G4 structure was identified in the promoter of the silk gland factor-1 gene (SGF1), which is the main regulatory gene for silk production in Bombyx mori. In this study, a BmSGF1 G4−/− homozygous mutant was generated with the G4 sequence knocked out. The promoter activity of BmSGF1 was lowered in the BmSGF1 G4−/− mutant. Pyridostatin (PDS) stabilized the G4 structure and increased the promoter activity of BmSGF1, whereas anti-sense oligonucleotide (ASO) complementary to the G4 sequence suppressed the promoter activity of BmSGF1. Compared with wild-type larvae, the deletion of the BmSGF1 G4 structure decreased both the expression of BmSGF1 and the fibroin heavy chain gene BmFib-H in the posterior silk gland and the weight of the cocoons. Overall, these results suggest that the promoter G4 structure of BmSGF1 participates in the transcription regulation of the BmSGF1 gene in the silkworm.

  • ORIGINAL ARTICLE
    Li Hou , Siyuan Guo , Yuanyuan Wang , Shaoye Liu , Xianhui Wang
    2024, 31(5): 1453-1465. https://doi.org/10.1111/1744-7917.13321

    Fat body metabolism plays crucial roles in each aspect of insect life traits. Although neuropeptides have been documented to be one of the major neuroendocrinal regulators involved in fat body metabolism, the detailed regulatory mechanism is poorly explored. Here, we conducted comparative metabolome and transcriptome analyses of fat body between wide type (WT) and adipokinetic hormone/corazonin-related peptide (ACP) loss of function mutants of the migratory locust,Locusta migratoria. We found that knockout of ACP resulted in significantly reduced fat body triacylglycerol content but enhanced abundance of phospholipids, particularly phosphatidylcholine and phosphatidylethanolamine. Additionally, the expression levels of genes involved in triacylglycerol and phospholipid synthesis and degradation were significantly altered in the fat body of ACP mutants. Moreover, female ACP mutants displayed much higher fecundity compared to WT females. These findings highlight the important role of neuropeptide ACP in fat body lipid metabolism homeostasis in locusts.

  • ORIGINAL ARTICLE
    Jernej Polajnar , Elizaveta Kvinikadze , Adam W. Harley , Igor Malenovský
    2024, 31(5): 1466-1476. https://doi.org/10.1111/1744-7917.13322

    Psyllids, or jumping plant lice (Hemiptera: Sternorrhyncha: Psylloidea), are a group of small phytophagous insects that include some important pests of crops worldwide. Sexual communication of psyllids occurs via vibrations transmitted through host plants, which play an important role in mate recognition and localization. The signals are species-specific and can be used to aid in psyllid taxonomy and pest control. Several hypotheses have been proposed for the mechanism that generates these vibrations, of which stridulation, that is, friction between parts of the forewing and thorax, has received the most attention. We have investigated vibrational communication in the European pear psyllid species Cacopsylla pyrisuga (Foerster, 1848) using laser vibrometry and high-speed video recording, to directly observe the movements associated with signal production. We describe for the first time the basic characteristics of the signals and signal emission of this species. Based on observations and analysis of the video recordings using a point-tracking algorithm, and their comparison with laser vibrometer recordings, we argue that males of C. pyrisuga produce the vibrations primarily by wing buzzing, that is, tremulation that does not involve friction between the wings and thorax. Comparing observed signal properties with previously published data, we predict that wing buzzing is the main mechanism of signal production in all vibrating psyllids.

  • ORIGINAL ARTICLE
    Huiting Zhao , Longlong Chen , Miaomiao Liu , Shuguo Zhao , Weihua Ma , Yusuo Jiang
    2024, 31(5): 1477-1488. https://doi.org/10.1111/1744-7917.13330

    Insulin receptors (InR) are an integral component of the insulin/insulin-like growth factor signaling pathway, which plays a vital role in insect development, lifespan, reproduction, and olfactory sensitivity. However, whether InR participate in the peripheral olfactory system of insects remains unclear. Recently, we found that 2-heptanone (2-HT) affects AcerInR expression, the gene for an InR protein, in Apis cerana cerana. We then examined the spatiotemporal expression profile of the gene in A. cerana cerana. The mRNA of AcerInR was primarily expressed in the antennae, wings, and legs of forager bees, which are probable chemosensory tissues. The results of fluorescence competitive binding assays, combined with site-directed mutagenesis, demonstrated that AcerOBP6 and AcerOBP14 exhibit strong binding affinities to 2-HT. Furthermore, after foragers were fed with double-stranded AcerInR, the expression levels of AcerOBP6 and AcerOBP14 decreased significantly, as did the electroantennogram responsiveness to 2-HT and some other odorants. In conclusion, our findings provide a foundation for understanding the involvement of AcerInR in the odor perception of A. cerana cerana. Moreover, they offer novel insights into the olfactory recognition mechanism in insects.

  • ORIGINAL ARTICLE
    William Jacob Pitt , William Rodney Cooper , Derek Pouchnik , Heather Headrick , Punya Nachappa
    2024, 31(5): 1489-1502. https://doi.org/10.1111/1744-7917.13327

    Aphids are phloem-feeding insects that reduce crop productivity due to feeding and transmission of plant viruses. When aphids disperse across the landscape to colonize new host plants, they will often probe on a wide variety of nonhost plants before settling on a host suitable for feeding and reproduction. There is limited understanding of the diversity of plants that aphids probe on within a landscape, and characterizing this diversity can help us better understand host use patterns of aphids. Here, we used gut content analysis (GCA) to identify plant genera that were probed by aphid vectors of potato virus Y (PVY). Aphids were trapped weekly near potato fields during the growing seasons of 2020 and 2021 in San Luis Valley in Colorado. High-throughput sequencing of plant barcoding genes, trnF and ITS2, from 200 individual alate (i.e., winged) aphids representing nine vector species of PVY was performed using the PacBio sequencing platform, and sequences were identified to genus using NCBI BLASTn. We found that 34.7&percnt, of aphids probed upon presumed PVY host plants and that two of the most frequently detected plant genera,Solanum and Brassica, represent important crops and weeds within the study region. We found that 75&percnt, of aphids frequently probed upon PVY nonhosts including many species that are outside of their reported host ranges. Additionally, 19&percnt, of aphids probed upon more than one plant species. This study provides the first evidence from high-throughput molecular GCA of aphids and reveals host use patterns that are relevant for PVY epidemiology.

  • ORIGINAL ARTICLE
    Xiao-Fei Li , Xing-Tao Qie , Bao-Tong Mo , Cai-Feng Wang , Zeng-Hua Xing , Jin-Yu Zhao , Chen-Zhu Wang , Chi Hao , Li Ma , Xi-Zhong Yan
    2024, 31(5): 1503-1518. https://doi.org/10.1111/1744-7917.13367

    Sex pheromones, which consist of multiple components in specific ratios promote intraspecific sexual communications of insects. Plutella xylostella (L.) is a worldwide pest of cruciferous vegetables, the mating behavior of which is highly dependent on its olfactory system. Long trichoid sensilla on male antennae are the main olfactory sensilla that can sense sex pheromones. However, the underlying mechanisms remain unclear. In this study, 3 sex pheromone components from sex pheromone gland secretions of P. xylostella female adults were identified as Z11-16:Ald, Z11-16:Ac, and Z11-16:OH in a ratio of 9.4 : 100 : 17 using gas chromatography – mass spectrometry and gas chromatography with electroantennographic detection. Electrophysiological responses of 581 and 385 long trichoid sensilla of male adults and female adults, respectively, to the 3 components were measured by single sensillum recording. Hierarchical clustering analysis showed that the long trichoid sensilla were of 6 different types. In the male antennae, 52.32%, 5.51%, and 1.89% of the sensilla responded to Z11-16:Ald, Z11-16:Ac, and Z11-16:OH, which are named as A type, B type, and C type sensilla, respectively; 2.93% named as D type sensilla responded to both Z11-16:Ald and Z11-16:Ac, and 0.34% named as E type sensilla were sensitive to both Z11-16:Ald and Z11-16:OH. In the female antennae, only 7.53% of long trichoid sensilla responded to the sex pheromone components, A type sensilla were 3.64%, B type and C type sensilla were both 0.52%, D type sensilla were 1.30%, and 1.56% of the sensilla responded to all 3 components, which were named as F type sensilla. The responding long trichoid sensilla were located from the base to the terminal of the male antennae and from the base to the middle of the female antennae. The pheromone mixture (Z11-16:Ald : Z11-16:Ac : Z11-16:OH = 9.4 : 100 : 17) had a weakly repellent effect on female adults of P. xylostella. Our results lay the foundation for further studies on sex pheromone communications in P. xylostella.

  • ORIGINAL ARTICLE
    Yongjie Zhang , Shulin He , Chengyin He , Ling Zhou , Ou Xu , Liang Qiao , Bin Chen , Yueqing Cao , Zhengbo He
    2024, 31(5): 1519-1532. https://doi.org/10.1111/1744-7917.13332

    The use of insecticides, primarily pyrethroids, is a pivotal strategy for mosquito control globally. Bioallethrin, the first commercially available volatile pyrethroid, can elicit spatial (i.e., noncontact) repellency to mosquitoes through the coactivation of olfactory receptor neurons and sodium channels. However, the olfactory mechanism of the repellency elicited by bioallethrin in mosquitoes is still unclear. Here, we demonstrated the involvement of AsOBP1 in the bioallethrin repellency in Anopheles sinensis, one of the main vectors of vivax malaria in China and other Southeast Asian countries. The behavioral and electrophysiological analyses in AsOrco−/− mutant found that the spatial repellency elicited by bioallethrin depended on the odorant receptor (OR)-mediated olfactory pathway. Furthermore, the repellency was reduced in the AsOBP1−/− mutant and a pyrethroid-resistant strain, in which the expression of AsOBP1 was significantly decreased. Moreover, recombinant AsOBP1 protein bound to bioallethrin in an in vitro competition assay. These results indicate that activation of the AsOBP1-mediated olfactory pathway is an important component of bioallethrin repellency. Our research lays the foundation for further elucidation into the olfactory mechanism of bioallethrin repellency and the behavioral modifications of pyrethroid-resistant mosquitoes.

  • ORIGINAL ARTICLE
    Caleb B. Hubbard , Amy C. Murillo
    2024, 31(5): 1533-1542. https://doi.org/0.1111/1744-7917.13326

    The house fly,Musca domestica, is a cosmopolitan species known for its pestiferous nature and potential to mechanically vector numerous human and animal pathogens. Control of adult house flies often relies on insecticides formulated into food baits. However, due to the overuse of these baits, insecticide resistance has developed to all insecticide classes currently registered for use in the United States. Field populations of house flies have developed resistance to imidacloprid, the most widely used neonicotinoid insecticide for fly control, through both physiological and behavioral resistance mechanisms. In the current study, we conducted a comprehensive analysis of the inheritance and dominance of behavioral resistance to imidacloprid in a lab-selected behaviorally resistant house fly strain. Additionally, we conducted feeding preference assays to assess the feeding responses of genetic cross progeny to imidacloprid. Our results confirmed that behavioral resistance to imidacloprid is inherited as a polygenic trait, though it is inherited differently between male and female flies. We also demonstrated that feeding preference assays can be instrumental in future genetic inheritance studies as they provide direct insight into the behavior of different strains under controlled conditions that reveal, interactions between the organism and the insecticide. The findings of this study carry significant implications for pest management and underscore the need for integrated pest control approaches that consider genetic and ecological factors contributing to resistance.

  • ORIGINAL ARTICLE
    Alitha Edison , Anja Michelbach , Dominique Sowade , Hanna Kertzel , Luise Schmidt , Martin Schäfer , Maximilian Hackhausen , Ralf Nauen , Pablo Duchen , Shuqing Xu
    2024, 31(5): 1543-1554. https://doi.org/10.1111/1744-7917.13319

    Agricultural pests can develop behavioral resistance to insecticides by choosing to feed or oviposit on insecticide-free hosts. As young larvae have relatively low mobility, oviposition preferences from female adults may play a critical role in shaping the evolutionary trajectory of pest populations. While oviposition avoidance of insecticide-treated hosts was found in different agriculture pests, it remains unclear whether female adults actively choose to occupy insecticide-free hosts. To address this question, we investigated feeding and oviposition preferences between imidacloprid-treated and imidacloprid-free plants in the Colorado potato beetle,Leptinotarsa decemlineata Say, a major potato pest. We performed behavioral choice assays on two strains that differed in both fecundity and insecticide resistance. We found that one strain preferred to feed on the insecticide-free plants and that this preference is not innate. Meanwhile, the other strain chose plants for feeding and oviposition randomly. Further analyses of the moving patterns of the beetles suggested that the oviposition preference in the first strain is likely due to active learning.

  • ORIGINAL ARTICLE
    Zheng-Wu Wang , Jin Zhao , Guang-Yun Li , Die Hu , Zi-Guo Wang , Chao Ye , Jin-Jun Wang
    2024, 31(5): 1555-1568. https://doi.org/10.1111/1744-7917.13315

    Aphids, the important global agricultural pests, harbor abundant resources of symbionts that can improve the host adaptability to environmental conditions, also control the interactions between host aphid and natural enemy, resulting in a significant decrease in efficiency of biological control. The facultative symbiont Serratia symbiotica has a strong symbiotic association with its aphid hosts, a relationship that is known to interfere with host–parasitoid interactions. We hypothesized that Serratia may also influence other trophic interactions by interfering with the physiology and behavior of major predators to provide host aphid defense. To test this hypothesis, we investigated the effects of Serratia on the host aphid Acyrthosiphon pisum and its predator, the ladybeetle Propylaea japonica. First, the prevalence of Serratia in different A. pisum colonies was confirmed by amplicon sequencing. We then showed that harboring Serratia improved host aphid growth and fecundity but reduced longevity. Finally, our research demonstrated that Serratia defends aphids against P. japonica by impeding the predator’s development and predation capacity, and modulating its foraging behavior. Our findings reveal that facultative symbiont Serratia improves aphid fitness by disrupting the predation strategy of ladybeetle larvae, offering new insight into the interactions between aphids and their predators, and providing the basis of a new biological control strategy for aphid pests involving the targeting of endosymbionts.

  • ORIGINAL ARTICLE
    Yunru Chen , Na Yu , Shuchen Dong , Guanqun Li , Huiya Pan , Zonglei Guo , Zewen Liu
    2024, 31(5): 1569-1578. https://doi.org/10.1111/1744-7917.13329

    Maternal care is critically important for the survival of offspring in various animals. Spiders in the family Lycosidae are known for their hunting ability and maternal care behaviors. Predation on newly hatched spiderlings (pulli) by mother spiders decreases when they come into contact, and they carry the pulli on their dorsal surface. However, the factors inducing maternal care in lycosid spiders have not been elucidated. In this study, we investigated maternal care in Pardosa pseudoannulata (Araneae, Lycosidae) females. We proposed that the physical interaction between pulli and mother spiders induces maternal care via m-aminophenylacetylene (m-A), a novel regulator of maternal care. The presence of pulli on the dorsal abdomen of non-mother spiders suppressed pulli predation and increased the pulli-carrying rate, and the absence of pulli on the mother spiders increased pulli predation and decreased the pulli-carrying rate. The compound m-A was abundant in mother spiders, and it could be induced in non-mother spiders when they carried pulli. The topical application of m-A to non-mother spiders and m-A injection decreased pulli predation and increased the pulli-carrying rate, respectively; these findings indicate that m-A in both internal tissues and the integument is required for the induction of maternal care behavior, and the interaction between pulli and females induces the production of m-A. In-depth study of the regulatory mechanism of maternal care will enhance our understanding of spider biology and behavior.

  • ORIGINAL ARTICLE
    Shovon Chandra Sarkar , Stephen Paul Milroy , Wei Xu
    2024, 31(5): 1579-1590. https://doi.org/10.1111/1744-7917.13328

    The tomato potato psyllid,Bactericera cockerelli, is an invasive pest in Australia, which can cause severe economic loss in the production of Solanaceous crops. As an invasive pest,B. cockerelli may also modify biotic interactions in Australian agricultural and native ecosystems. Resident generalist predators in an area may have the ability to utilize invasive pest species as prey but this will depend on their specific predatory behavior. The extent to which generalist predators learn from their previous dietary experience (i.e., whether they have used a particular species as prey before) and how this impacts subsequent prey choice will influence predator and prey population dynamics after invasion. In this study, one nonnative resident ladybird,Hippodamia variegata, and one native ladybird,Coccinella transversalis, were investigated. Dietary experience with B. cockerelli as a prey species significantly increased preference for the psyllid in a short term (6 h) Petri dish study where a choice of prey was given. Greater suppression of B. cockerelli populations by experienced ladybirds was also observed on glasshouse grown tomato plants. This was presumably due to altered prey recognition by experience. The result of this study suggest the potential to improve the impact of biological control agents on invasive pests by providing early life experience consuming the target species. It may prove valuable for developing improved augmentative release strategies for ladybirds to manage specific insect pest species.

  • ORIGINAL ARTICLE
    Laura Marcela Martinez-Chavez , Joe M. Roberts , Alison J. Karley , Bethan Shaw , Tom W. Pope
    2024, 31(5): 1591-1602. https://doi.org/10.1111/1744-7917.13316

    Behavior and fitness are important ecological traits frequently measured in insect bioassays. A common method to measure them in soft-bodied herbivorous insects involves confining individuals to plant leaves using clip cages. Although studies have previously highlighted the negative effects of clip cages on leaf physiology, little is known about the impact that using this confinement method has on insect fitness. The responses of different aphid genotypes/clones to different containment methods have not previously been investigated. Here we measured key fitness traits (intrinsic rate of natural increase, mean relative growth rate, time to reach reproductive adulthood and population doubling time) in the potato aphid,Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae), when confined to plants using two methods: (1) clip cages to confine aphids to individual strawberry leaves and (2) a mesh bag to confine aphids to whole strawberry plants. Our study identified a strong negative impact on all the measured aphid fitness traits when using clip cages instead of mesh bags. We also identified genotype-specific differences in response to confinement method, where clip cage confinement differentially affected the fitness of a given aphid genotype compared to the same genotype on whole plants. These results suggest that clip cage use should be carefully considered when experiments seek to quantify insect fitness and that whole plants should be used wherever possible. Given the prevalence of clip cage use in insect bioassays, our results highlight the need for caution when interpreting the existing literature as confinement method significantly impacts aphid fitness depending on their genotype.

  • ORIGINAL ARTICLE
    Zeshi Qin , Yixia Cao , Yan Wang , Jun Ding , Wujia Xia , Juan Shi
    2024, 31(5): 1603-1616. https://doi.org/10.1111/1744-7917.13335

    Using stable isotopes to detect and analyze the geographical origin of insects represents an important traceability technology, which requires a rich isotope database. In this study, we representatively sampled the Chinese provinces where flighted spongy moth complex (FSMC) has been reported and, for the first time, used co-kriging interpolation to predict the distribution patterns of FSMC δ13C values in the main distribution areas. From 2020 to 2022, we set up 60 traps in 12 provinces and cities in China and collected 795 FSMCs. Then, 6 main climatic factors were obtained by multi-collinearity screening from 21 types of meteorological data collected at the sample plots, and a correlation analysis was carried out by combining longitude, latitude, and altitude data with the δ13C values of FSMC. Next, we performed a co-kriging interpolation using the 2 climatic factors with the highest correlation (isothermality and altitude) and the δ13C values of FSMC. A cross-validation was performed to systematically test 11 candidate models and select the best semi-variogram model (“Exponential”), which was then used to build a co-kriging interpolation model. The geographical distribution patterns of the FSMC δ13C values obtained from the 2 interpolation models (i.e., interpolated with isothermality and altitude, respectively) were almost the same. Moreover, the δ13C values varied significantly at the regional scale, showing regular changes in spatial distribution. Overall, the reference indicator map of the δ13C values generated from stable isotopes can be used to greatly improve the efficiency of discrimination analyses on the geographical origin of FSMC.

  • ORIGINAL ARTICLE
    Hongran Li , Yan Peng , Chao Wu , Zhimin Li , Luming Zou , Kaikai Mao , Junfen Ping , Ryan Buck , Scott Monahan , Arun Sethuraman , Yutao Xiao
    2024, 31(5): 1617-1630. https://doi.org/10.1111/1744-7917.13320

    Understanding the genetic basis of adaptive evolution following habitat expansion can have important implications for pest management. The pink rice borer (PRB),Sesamia inferens (Walker), is a destructive pest of rice that was historically restricted to regions south of 34° N latitude in China. However, with changes in global climate and farming practices, the distribution of this moth has progressively expanded, encompassing most regions in North China. Here, 3 highly differentiated subpopulations were discovered using high-quality single-nucleotide polymorphism and structural variant datasets across China, corresponding to northern, southern China regions, and the Yunnan-Guizhou Plateau, with significant patterns of isolation by geographic and environmental distances. Our estimates of evolutionary history indicate asymmetric migration with varying population sizes across the 3 subpopulations. Selective sweep analyses estimated strong selection at insect cuticle glycine-rich cuticular protein genes which are associated with enhanced desiccation adaptability in the northern group, and at the histone-lysine-N-methyltransferase gene associated with range expansion and local adaptation in the Shandong population. Our findings have significant implications for the development of effective strategies to control this pest.

  • ORIGINAL ARTICLE
    Huiling Sang , Yancan Li , Shuxin Tan , Pu Gao , Bei Wang , Shengnan Guo , Shudong Luo , Cheng Sun
    2024, 31(5): 1631-1644. https://doi.org/10.1111/1744-7917.13324

    Bumblebees are a genus of pollinators (Bombus) that play important roles in natural ecosystem and agricultural production. Several bumblebee species have been recorded as under population decline, and the proportion of species experiencing population decline within subgenus Thoracobombus is higher than average. Bombus opulentus is 1 species in Thoracobombus, but little is known about its recent population dynamics. Here, we employed conservation genomics methods to investigate the population dynamics of B. opulentus during the recent past and identify the likely environmental factors that may cause population decline. Firstly, we placed the scaffold-level of B. opulentus reference genome sequence onto chromosome-level using Hi-C technique. Then, based on this reference genome and whole-genome resequencing data for 51 B. opulentus samples, we reconstructed the population structure and effective population size (Ne) trajectories of B. opulentus and identified genes that were under positive selection. Our results revealed that the collected B. opulentus samples could be divided into 2 populations, and 1 of them experienced a recent population decline; the declining population also exhibited lower genetic diversity and higher inbreeding levels. Genes related to high-temperature tolerance, immune response, and detoxication showed signals of positive selection in the declining population, suggesting that climate warming and pathogen/pesticide exposures may contribute to the decline of this B. opulentus population. Taken together, our study provided insights into the demography of B. opulentus populations and highlighted that populations of the same bumblebee species could have contrasting Ne trajectories and population decline could be caused by a combination of various stressors.

  • ORIGINAL ARTICLE
    Yingying Cui , Jérémie Bardin , Benjamin Wipfler , Alexandre Demers-Potvin , Ming Bai , Yi-Jie Tong , Grace Nuoxi Chen , Huarong Chen , Zhen-Ya Zhao , Dong Ren , Olivier Béthoux
    2024, 31(5): 1645-1656. https://doi.org/10.1111/1744-7917.13338

    Until the advent of phylogenomics, the atypical morphology of extant representatives of the insect orders Grylloblattodea (ice-crawlers) and Mantophasmatodea (gladiators) had confounding effects on efforts to resolve their placement within Polyneoptera. This recent research has unequivocally shown that these species-poor groups are closely related and form the clade Xenonomia. Nonetheless, divergence dates of these groups remain poorly constrained, and their evolutionary history debated, as the few well-identified fossils, characterized by a suite of morphological features similar to that of extant forms, are comparatively young. Notably, the extant forms of both groups are wingless, whereas most of the pre-Cretaceous insect fossil record is composed of winged insects, which represents a major shortcoming of the taxonomy. Here, we present new specimens embedded in mid-Cretaceous amber from Myanmar and belonging to the recently described species Aristovia daniili. The abundant material and pristine preservation allowed a detailed documentation of the morphology of the species, including critical head features. Combined with a morphological data set encompassing all Polyneoptera, these new data unequivocally demonstrate that A. daniili is a winged stem Grylloblattodea. This discovery demonstrates that winglessness was acquired independently in Grylloblattodea and Mantophasmatodea. Concurrently, wing apomorphic traits shared by the new fossil and earlier fossils demonstrate that a large subset of the former “Protorthoptera” assemblage, representing a third of all known insect species in some Permian localities, are genuine representatives of Xenonomia. Data from the fossil record depict a distinctive evolutionary trajectory, with the group being both highly diverse and abundant during the Permian but experiencing a severe decline from the Triassic onwards.

  • CORRECTION
    2024, 31(5): 1657-1660. https://doi.org/10.1111/1744-7917.13331