The oriental armyworm genome yields insights into the long-distance migration of noctuid moths

Authors: TONG, DANDAN - Chinese Academy Of Agricultural Sciences; ZHANG, LEI - Chinese Academy Of Agricultural Sciences; WU, NINGNING - Chinese Academy Of Sciences; XIE, DIANJIE - Chinese Academy Of Agricultural Sciences; FANG, GANGQI - Chinese Academy Of Sciences; Coates, Brad; Sappington, Thomas; LIU, YUEQIU - Beijing University Of Agriculture; CHENG, YUNXIA - Chinese Academy Of Agricultural Sciences; XIA, JIXING - Chinese Academy Of Agricultural Sciences; JIANG, XINGFU - Chinese Academy Of Agricultural Sciences; ZHAN, SHUAI - Chinese Academy Of Sciences

Submitted to: Cell Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/25/2022
Publication Date: 12/20/2022
Citation: Tong, D., Zhang, L., Wu, N., Xie, D., Fang, G., Coates, B.S., Sappington, T.W., Liu, Y., Cheng, Y., Xia, J., Jiang, X., Zhan, S. 2022. The oriental armyworm genome yields insights into the long-distance migration of noctuid moths. Cell Reports. 41(12). Article 111843. https://doi.org/10.1016/j.celrep.2022.111843.
DOI: https://doi.org/10.1016/j.celrep.2022.111843

Interpretive Summary: Patterns of seasonal migration by some pest insects impact the geographic range and severity of crop damage. These movements also affect the spread of genes that adapt to climatic shifts or producer control practices. The oriental armyworm is a severe pest of multiple crops throughout much of east Asia and is a model for insect migratory behavior. This moth makes annual migrations from southern locations to infest and damage crops in northern locations during spring and summer months, and engages in a return migration in the fall. Larvae that are crowded on host plants turn dark, develop rapidly, and are more likely to migrate as adults than those that develop under uncrowded conditions. ARS scientists along with a team of collaborators developed an oriental armyworm genome sequence assembly as a tool to understand the genetic basis of development and behaviors in migratory pest insects. This work showed that genes involved in dark pigment formation are more highly expressed in larvae grown in crowded conditions. Additionally, genes involved in producing a hormone that affects flight behavior are more highly expressed in migrant compared to non-migrant adults. Suppression of genes involved in producing this hormone in migrating adults caused a switch to non-migratory behavior, the same switch that can happen in the wild in response to environmental cues experienced by a young adult. The expression of genes involved in sensing the earth’s magnetic field in migrating adults peaked during nighttime hours and may partially explain how moths navigate at night when visual cues are lacking. This research is important for understanding the genetics of insect migration, including that of true armyworm, a closely related pest species in the U.S. This information will be useful to regulators, and government and university scientists concerned about the impacts of migratory insect populations on crop production and in developing tactics to predict migratory pest outbreaks.

Technical Abstract: The oriental armyworm, Mythimna separata, is one of the world’s most devastating pests of cereal crops. This moth is a multigenerational roundtrip migrant, moving long distances between its southern overwintering and northern breeding ranges in China, and serves as a model species for other migratory insects. We integrated genomic, transcriptomic, gene editing and behavior experiments to better understand mechanisms governing M. separata’s migratory adaptations and behavior. We assembled a chromosome scale genome and present a draft 694.7-Mb genome containing a set of 16,968 protein-coding genes. Demographic history demonstrates that the migratory population of M. separata has undergone successive contractions, suggesting a diet-mediated bottleneck in line with the emergence of farming civilization. Although an agricultural pest of mainly graminaceous crops, the expansion of range in Lepidoptera receptors indicates M. separata has potential to adapt to various host plants in other families. Genes involved in larval epidermis melanization regulate larval development into dark gregarious or light solitary morphs associated with migratory or resident adults, respectively. Juvenile hormone (JH) pathway genes were responsible adult plasticity of reproduction, with higher expression of allatotropin (AT) gene when adults flown at appropriate flight mode, accelerating adults laying eggs but not reducing lifetime fecundity. Magnetosensing protein of magnetoreceptor (MagR) and cryptochrome (CRY) help migrants navigate via geomagnetic field. Our reported genomic resources and findings enhances our understanding of the genetic and molecular insight into long-distance migration in pests.