Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), the fall armyworm (FAW), is a highly polyphagous invasive pest that originated in tropical and subtropical America and has quickly migrated to Asia and Africa(Rioba and Stevenson, 2020). FAW was initially discovered in China's Yunnan Province in December 2018, and it has since spread rapidly throughout the country, posing a severe economic danger to China's crop supply (Wang et al., 2020). Presently, FAW has been recorded from all but five provinces (municipalities) in the North West and North East in China that includes about 13 million hectares of corn(Li et al., 2021b). Unlike many migratory insect pests, FAW does not have the ability to diapause(Du Plessis et al., 2020), and cannot, therefore, withstand severe cold. FAW adult has a strong capability of long-distance migration, and the average flight distance was more than 100 km per night under proper environmental conditions (Tendeng et al., 2019), which aggravating its rapid spreading. Northern outbreaks of FAW start with reproduction in tropical and subtropical regions and disperse northward in the spring and summer, and migration to south to overwinter in autumn and winter in China(Huang et al., 2020; Li et al., 2021b).
Insects live in incredibly complex environments. The alimentary canal of insects is in constant contact with their environments, and a gatekeeper and coordinator of organism fitness and physiology (Colombani and Andersen, 2020). The gut microbiota takes participate in diverse aspects of insect physiology (Gomes et al., 2020). These microbial communities are diverse and large in number; they form a microbial ecosystem in the gut, some of which are beneficial and some harmful to the host(Shin et al., 2011; Storelli et al., 2011). The microbial communities of gut is a pivotal endocrine system and affects a broad range of physiological functions including providing nutrients(Thong-On et al., 2012); the efficiency of disease transmission by vector insect(Cirimotich et al., 2011a; Cirimotich et al., 2011b); the degradation of toxic compounds(Ceja-Navarro et al., 2015); protect the host from insecticides, parasites and pathogens (Kalappa et al., 2018; Su et al., 2019) or accelerate pathogens infection(Yuan et al., 2021); and promote host growth and development(Shin et al., 2011). The diversity and abundance of microbial communities of gut are directly affected by many factors, such as lifestyle, dietary patterns, pesticidal usage, age, gender, and the host genotype(Behar et al., 2008; Chen et al., 2018b; Chen et al., 2020).
In recent years, a large number of insect microbial communities have been discovered, including fruit flies (Erkosar et al., 2017; Bing et al., 2018), mosquitoes (Kang et al., 2020; Alvarado et al., 2021), locusts(Dillon et al., 2010; Tan et al., 2021), as well as in lepidopteran pests, such as Bombyx mori (Chen et al., 2018a; Chen et al., 2018b; Zhang et al., 2021), Spodoptera littoralis(Chen et al., 2016), Spodoptera exigua caterpillars(Martinez-Solis et al., 2020), and Helicoverpa zea (Deguenon et al., 2021). Of which, the gut microbiota of S. frugiperda has been gradually studied in recent years. Such as, many researches focused on the gut bacterial communities of S. frugiperda raised on different host plants, diets, or transgenic plants(Abdelgaffar et al., 2019; Jones et al., 2019; Mason et al., 2020; Lv et al., 2021), some compared the gut microbiota composition of susceptible and insecticide-resistant S. frugiperda strains(Gomes et al., 2020), some studies found antibiotic, seasonal variations and parasitoid also can alter the gut microbiome in the larvae(Chen et al., 2021; Palacio et al., 2021; Wang et al., 2021), few researchers characterized the diversity of bacteria associated with populations of S. frugiperda in particular region or country(Gichuhi et al., 2020). While, little is known about the compositional and functional variations of gut microbiota between captive and wild S. frugiperda, particularly along the autumn and winter migration route in China.
In addition, very little is known about whether S. frugiperda responses to the complex field environment at the molecular level, especially the immune system. Insects have a complicated immune system that allows them to respond efficiently to a variety of pathogens and infections(Hoffmann, 1995). In general, pathogens invade insects may through the gut if present in ingested food; or they may enter the hemolymph on the body surface, or by penetrating the integument or gut tissues (Wu et al., 2016). The integument and peritrophic membrane, as physical barriers, are ability to prevent infection by pathogens (Chen and Lu, 2018). Once this barrier is breached, the insect innate immune system is activated to prevent pathogen growth and dissemination inside the infected insect(Hoffmann, 2003; Hultmark, 2003). Humoral immune reactions involve activation of prophenol oxidase (PPO) to phenol oxidase (PO), rely more heavily on the Toll, Imd and Jak/Stat immune pathways and on melanization and expression of various genes involved in antimicrobial peptides (AMPs) along with different challenges.
Here, we explored the impacts of habitats with dietary and environmental change on the diversity and composition of gut microbiota and the immune genes expression in wild and captive FAWs. The captive strains were fed on wheat or corn that are mainly crops in the route of south migration of S. frugiperda in the autumn and winter in Jianghuai region, China. We selected the wild strains along the Huaihe River and Yangtze River in the JiangHuai region, China. We studied the gut microbiota diversity and function and immune genes expression in both wild and captive S. frugiperda populations to learn more about: (1) the diversity and composition of gut microbiota among different strains; (2) the functional differences in the gut microbiota between captive and wild FAWs; and (3) the immune genes response to the FAWs' natural habitats. The main hypothesis of our study was that the field environments had a significant impact on shaping the bacterial community and immune genes of the circulating S. frugiperda in the autumn and winter migration routes in China. This study will provide better understanding of the microbial ecology and the innate immunity of S. frugiperda and the role of environments in mediating gut microbe interactions and immune responses, and is a useful foundation for exploring pest-filed interactions that could be exploited to improve the efficient control measures.