Adaptation strategies of insects to their environment by collecting and utilizing external microorganisms

Insects adjust their adaptive capacity to biotic and abiotic stresses by collecting and utilizing microorganisms from the environment and diet. Insects and microorganisms are ubiquitous in almost all ecosystems and contribute significantly to ecosystem stability (Schowalter et al. 2018; Crespo-Pérez et al. 2020; Sun et al. 2023; Sveen et al. 2023). Due to climate change and human activities, insects are constantly exposed to emerging stresses, compelling them to develop physiological, behavioral, and morphological adaptations to withstand these challenges (Behmer 2009; Sheikh et al. 2017; Xiong 2022; Bai et al. 2023). While genomic evolution and natural selection are stable strategies for accumulating these changes, the processes often take thousands or even millions of years (Lamichhaney et al. 2015; Lamichhaney et al. 2016; Nuismer et al. 2022), making it challenging for insects to adapt swiftly to these stresses. There are long-term and dynamic interactions between insects and associated microorganisms, which are readily incorporated into insect bodies or onto their body surfaces and are extensively involved in various physiological activities of the host (Douglas 2015; Hosokawa & Fukatsu 2020). Generally, these sites on insects are inhabited by diverse microorganisms, leading to extensive competition among them. Thus, insects can theoretically exploit the competition among microorganisms to enhance their fitness and adaptability. Indeed, recent studies have discovered similar cases, providing new insights into the diverse functions of insect-associated microorganisms in insect adaption (Fig. 1). Under normal circumstances, gut-beneficial microbes can outcompete harmful ones and perform functions that aid the host, including breaking down complex nutrients, fostering growth and development, and detoxifying harmful compounds (Tellez et al. 2006; Kikuchi et al. 2012; Jordan & Tomberlin 2021; Zhang et al. 2024c). For instance, changes in the gut microbial composition of Bactrocera dorsalis affect insect metabolism and transcriptional regulation, thereby promoting growth (Wang et al. 2023). They also shape gut-associated lymphoid tissue assembly, educate the immune system, impact intestinal mucosal barrier integrity (Tellez et al. 2006; Xu et al. 2018), and enhance the insect's ability to detoxify plant-released defense chemicals (Pincebourde et al. 2017; Salem et al. 2020; Wang et al. 2020). Several microorganisms derived from silkworm guts exhibit probiotic potential and enhance insect resistance to diseases and toxins, including insecticides (Jordan & Tomberlin 2021; Liang et al. 2022; Zhang et al. 2022). However, as mentioned earlier, the survival environment of insects is constantly changing, especially for invasive insects whose living environments often undergo drastic changes during the invasion process. Some microorganisms that can respond to these changes along with the host insect may rapidly increase in abundance and aid the host. Recently, Zhang et al. found that Hyphantria cunea can recruit gut microorganisms (Bacteroides, Blautia, and Coprococcus) to help adapt to the new host plant, Metasequoia glyptostroboides, in its expansion range in southern China (Zhang et al. 2024a). This suggests that adjusting the abundance of gut microorganisms in insects provides an alternative strategy to rapidly adapt to the new host plants or environments and promotes their fitness (Fig. 1). The insect cuticle is another arena for various insect-associated microorganisms to thrive. The insect's environment is thought to be the primary source of the composition of cuticle microorganisms. For instance, insects reared on plants harbor microorganisms on their cuticle that are mainly derived from their host plants (Zhao et al. 2024), whereas the ectomicrobiome of adult Drosophila melanogaster reared in vials consists mainly of bacteria from their excreta (Hong et al. 2022). On the other hand, entomopathogenic fungi can infect insects directly by penetrating the cuticle, and certain microorganisms residing in the cuticle of insect epidermis unsurprisingly contribute to defense against these fungal pathogens by producing antibiotics and competing for nutrients and survival space on the insect body surface (Levy et al. 1992; Currie et al. 1999; Legrifi et al. 2022). However, it is surprising that insects can "intentionally" carry and enrich beneficial microorganisms that can inhibit pathogenic fungi. For example, Zhao et al. found that the bacterium Mammaliicoccus sciuri, isolated from the silkworm's cuticle, completely inhibited spore germination and inhibited the penetration of entomopathogenic fungi, Metarhizium robertsii and Beauveria bassiana, by secreting enzymes that destroy fungal spores (Zhao et al. 2024). Notably, this microorganism is exclusively found in host plant mulberry leaves and can rapidly re-colonize the insect's cuticle after being lost during molting. Another example involves fungus-growing ants carrying a filamentous bacterium (actinomycete) in the Streptomyces genus on their cuticle, which produces a cyclic depsipeptide (dentigerumycin) targeting the specialized garden-parasite Escovopsis (Currie et al. 1999; Oh et al. 2009). Although frequent molting during insect growth and development removes most of the microorganisms from the cuticle, some insect cuticles have specialized pouch structures that can host ectomycorrhizal symbionts to seed bacterial cells post-molting (Janke et al. 2022), which then facilitates rapid recombination of these ectomicrobiomes. Even insects without such structures have been shown to gather surrounding microorganisms into their cuticle to resist fungal pathogens. This demonstrates that insects can exploit the competition among microorganisms for their benefit, but more cases remain to be discovered. Understanding how insects harness microorganisms to withstand adverse environmental conditions is crucial for both theoretical studies and practical applications. On the one hand, it provides a foundation for understanding how insects adapt to the environment by recruiting beneficial microorganisms. On the other hand, disrupting or manipulating the equilibrium between insects and their associated microorganisms could facilitate effective pest control and safeguard crops. Additionally, isolating or extracting beneficial microorganisms from insects can be applied in food, medical, and other industries to improve overall quality of life (Kerr 1999). Some insect-associated microorganisms have already been developed for pest control (Tu et al. 2023; Zhang et al. 2023; Ma et al. 2024), ecological regulation (Douglas 2015; Coolen et al. 2022; Picciotti et al. 2023; Zhang et al. 2024b), drug discovery (Chevrette et al. 2019; van Moll et al. 2021; Baranova et al. 2022), and biomass decomposition (Skelton et al. 2019; Diksha et al. 2022). Future research directions should explore the temporal and spatial transmission of insect-associated microorganisms within or outside of insects and their essential components or pathways that facilitate insect adaptation (Fig. 1). This research was supported by the National Natural Science Foundation of China (32160666 and 32370523) and the Guizhou Province Science and Technology Support Project ([2022] General 239).