The Microbiome as a Driver of Insect Physiology, Behavior, and Control Strategies

Abstract

Insect pests impose major economic, agricultural, and public health burdens, damaging crops and transmitting pathogens such as dengue, malaria, and Zika. Conventional chemical control is increasingly ineffective due to insecticide resistance and environmental concerns, prompting a search for innovative strategies. The insect microbiome—comprising both obligate symbionts and environmentally acquired microbes—emerges as a key driver of host physiology and behavior. Microbes influence nutrient acquisition, immunity, reproduction, and chemosensory processing, often to promote their own transmission. By modulating olfactory and gustatory pathways, microbiota can alter host-seeking, mate choice, foraging, and oviposition patterns, reshaping ecological interactions and vector dynamics. These effects are shaped by microbial acquisition routes, habitat conditions, and anthropogenic pressures such as pesticide use, pollution, and climate change. Understanding these multi-directional interactions offers opportunities to design highly specific, microbe-based insect control strategies, from deploying microbial metabolites that disrupt host sensory systems to restoring beneficial symbionts in threatened pollinators. Integrating microbiome ecology with insect physiology and behavior not only deepens our understanding of host–microbe coevolution but also enables the development of sustainable, targeted alternatives to chemical insecticides. This review synthesizes current evidence linking microbiomes to insect biology and explores their potential as tools for pest and vector management.

1. Introduction

Microbes influence insect biology and physiology both directly—through effects on metabolism, immunity, chemosensation, and reproduction—and indirectly, by altering the chemical ecology of plants, water, or other substrates that insects use [1,2,3]. Many insect-associated microbes exploit their hosts as vectors for viruses, resistance genes, and for their own proliferation, while in return providing nutrients, immune protection, and chemosensory modulation necessary for host survival [4,5,6]. Understanding the mechanisms underlying these interactions is essential for developing innovative insect control strategies to protect agriculture and human health [7,8]. Rather than relying solely on the “sterilized organism” approach, it is now possible to envision interventions that manage plant and environmental microbiomes to either preserve beneficial symbioses or disrupt harmful ones [9,10]. Microbial enzymes and volatile organic compounds could be harnessed to deter pests or their predators and pathogens [11,12]. Peptide-based topicals that mimic microbial signaling molecules could modulate host behavior or immunity [13,14]. With climate change threatening microbial diversity, microbiome restoration may also reduce disease transmission risk [15,16]. Ultimately, the ecological consequences of the multi-way interactions between microbes, insects, their habitats, and environmental factors must be understood to inform the design of microbe-based pest control.

2. The Burden of Insect Pests and Vectors

Insect pests impose a substantial global burden on agriculture, biodiversity, and public health. Agricultural pests are responsible for extensive crop damage, estimated to cause annual losses exceeding USD 70 billion worldwide, not only reducing yields but also driving declines in plant biodiversity and contributing to greenhouse gas emissions through altered land use and increased reliance on agricultural inputs [15,17]. Invasive insect species exacerbate this impact by outcompeting native species, altering trophic networks, and introducing new pathogens [18].

Vector-borne diseases transmitted by insects—including malaria, dengue, Zika, chikungunya, yellow fever, and West Nile virus—account for more than 700,000 human deaths annually and collectively cost billions in healthcare expenditures and productivity losses [17,19,20]. Climate change, rapid urbanization, and intensifying global trade are expanding the geographic range and seasonal activity of many insect vectors, increasing the risk of outbreaks in previously unaffected regions [21,22,23].

Current control strategies rely heavily on chemical insecticides, which, despite their effectiveness, carry significant drawbacks: environmental contamination, non-target organism toxicity, and the accelerating evolution of insecticide resistance [24,25]. The widespread use of pyrethroids, organophosphates, and neonicotinoids has selected for resistant populations in multiple vector and pest species, eroding the long-term efficacy of chemical interventions [26,27]. The urgent need for new, sustainable control strategies has turned attention toward alternative approaches, including microbial symbionts and their metabolites, which may offer high specificity and reduced ecological disruption.

Recent advances have revealed that insect-associated microbes are not merely passive passengers but active modulators of host physiology, influencing processes such as nutrient acquisition, immunity, reproduction, and sensory perception [1,4]. Of particular interest is their role in shaping insect chemosensory systems—critical for foraging, mate choice, oviposition site selection, and host-seeking in vector species [28]. Understanding how these microbes are acquired, and whether their presence correlates with host chemosensory gene expression, could illuminate the mechanisms by which microbes shape insect sensory behavior.

3. Composition, Acquisition, and Roles of the Insect Microbiome

The insect microbiome is taxonomically diverse and functionally integral to host biology. It encompasses both obligate symbionts—comprising the insect’s “core microbiome”—and facultative or environmentally acquired microbes. Obligate symbionts are typically transmitted vertically from parent to offspring and are indispensable for normal development, reproduction, and survival [1,29,30]. Most microbial colonization in disease vectors occurs during early developmental stages, particularly the larval phase, when hosts encounter a wide range of environmental and dietary microorganisms [2,31,32]. In addition to vertical and environmental acquisition, horizontal gene transfer (HGT) is a mechanism through which insects and their symbionts gain novel traits, some of which become permanently integrated into host biology.

Internal microbiomes, often localized in the gut, bacteriocytes, or reproductive tissues, harbor specialized symbionts that contribute to nutrient provisioning [33], immune system maturation [34,35], and behavioral modulation [36] alongside environmentally acquired taxa. Gut bacteria can also suppress vector competence for pathogens—limiting the ability of insects like mosquitoes, sandflies, or triatomines to transmit disease—thereby indirectly promoting their own dissemination in host populations [34,37,38,39].

External microbiomes are largely environmentally derived and highly variable across habitats, diets, and geographic ranges [40,41]. Dietary intake is a major route of microbial acquisition: herbivorous insects consuming leaves, nectar, pollen, or phloem sap inevitably ingest plant-associated microorganisms, including epiphytic bacteria, endophytes, and yeasts [42,43,44]. Some survive gut passage, colonize internal tissues, or transiently modulate physiological pathways. Plant-associated microbes can influence digestion [9,45,46], nutrient assimilation [2], detoxification [47], and sensory perception [11,48]. They can also serve as vectors for horizontally transferred traits, facilitating rapid adaptation to novel ecological niches [49,50].

HGT introduces novel functions into host genomes or redistributes traits among symbionts. One of the most well-studied cases involves the lateral transfer of carotenoid biosynthesis genes from fungi to aphids, enabling endogenous pigment production and enhanced antioxidant capacity [51,52]. Similar processes have been reported for the acquisition of plant cell-wall-degrading pectinases from bacteria by stick insects, expanding host dietary breadth [53]. Symbiont-to-symbiont transfer also plays a critical role in shaping insect phenotypes; toxin cassettes carried by Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) secondary endosymbiont (APSE) bacteriophages are horizontally exchanged among Hamiltonella defensa Moran et al. (Enterobacterales: Enterobacteriaceae) strains, mediating aphid resistance to parasitoid wasps [54,55]. Moreover, transfers from Wolbachia into host chromosomes have been detected across multiple insect orders, in some cases involving large genomic tracts, highlighting the intimacy of host–symbiont genetic exchange [56,57,58]. Genome-scale surveys suggest that HGT is widespread and occasionally functionally integrated, influencing traits as diverse as immunity, reproduction, and even behavioral processes such as courtship [59,60,61,62]. These findings broaden the concept of “microbiome acquisition” to encompass gene-level assimilation and mobile element-mediated remodeling, processes that may stabilize nutritional, defensive, or sensory traits over evolutionary timescales and alter the adaptive trajectories of both pest and beneficial insects. These genetic exchanges complement the more transient microbial associations acquired from the environment, underscoring the multiple evolutionary routes through which insects and their symbionts establish long-term partnerships.

These symbioses have deep evolutionary roots. Insects have maintained microbial partnerships for over 400 million years, making them among the most ancient and stable animal–microbe associations known [2,4,63]. Nutrient-supplementing relationships are particularly consequential, with symbionts synthesizing essential amino acids, B vitamins, and sterols absent from the host’s natural diet [1,3,33]. Many also enhance host survival by degrading plant secondary metabolites [5], detoxifying insecticides [47,64,65], and producing antimicrobial compounds. For example, Streptomyces strains isolated from insects exhibit greater inhibitory activity against fungi and bacteria than their soil- or plant-associated relatives, reflecting adaptation to host-associated pathogen pressures [66,67].

Symbionts can also manipulate host reproduction—a strategy that enhances microbial transmission. For example, endosymbionts of scale insects can shift reproduction from haploid to haplodiploid systems [68], and Spiroplasma in Drosophila can cause male-killing, skewing sex ratios [69]. Among these, Wolbachia is one of the most widespread bacterial symbionts, infecting an estimated 40–60% of insect species [70,71]. Its effects are strain-, host-, and context-dependent, spanning alterations in fertility, mating behavior, locomotion, olfactory sensitivity, learning, and memory [72,73,74]. Cytoplasmic incompatibility—a hallmark Wolbachia phenotype—reduces fertility when infected males mate with uninfected females [75,76]. In Drosophila melanogaster Meigen (Diptera: Drosophilidae), Wolbachia induces expression of odorant-binding protein 28a (OBP28a), which in turn activates immune-associated genes, illustrating a direct link between microbial presence, sensory gene regulation, and immune readiness [35].

How microbiome composition is shaped by acquisition pathways and how these communities mechanistically influence insect physiology and behavior remains unclear. While certain behavioral effects—such as altered olfactory preferences, feeding patterns, or reproductive manipulation—have been linked to specific microbial taxa, the causal molecular pathways remain unresolved in most systems. Moreover, the relative importance of vertical versus environmental acquisition under changing climatic and anthropogenic pressures is poorly understood, leaving open questions about how rapidly host–microbe relationships can adapt. A mechanistic understanding of how microbiomes modulate insect sensory systems and fitness traits could enable the rational design of microbe-derived or microbiome-informed control strategies that are precise, ecologically sustainable, and minimally disruptive.

4. Microbial Modulation of Chemosensory Physiology

The insect microbiome can influence host sensory systems at a fundamental level, altering how insects perceive and respond to chemical cues in their environment. Through modulation of gene expression networks, microbial communities can affect immunity, sensory perception, and behavior in ways that often align with their own transmission and survival (Figure 1). Microbial diversity has been positively correlated with the expression of genes involved in immune cell development and interleukin-12 (IL-12) regulation, and negatively correlated with genes linked to inflammatory responses [3,77,78]. Similarly, variation in microbiome composition has been associated with the expression of genes related to chemoattraction, complement activation, and antibacterial activity, suggesting that microbial community structure can shape both immune readiness and sensory processing [3,77,78].

However, it is important to note that causality in these interactions is likely bidirectional. The physiological state of the host—including immune activation, endocrine signaling, and developmental stage—can strongly determine which microbes persist or are excluded. For example, immune effectors such as antimicrobial peptides and reactive oxygen species in the insect gut selectively shape microbial communities, restricting the growth of opportunists while maintaining core taxa [34,79,80]. Similarly, changes in hormonal signaling during molting or reproduction have been shown to restructure microbial assemblages in mosquitoes and Drosophila [31,81]. Nutritional physiology is also a key determinant; dietary shifts alter gut pH, enzyme profiles, and metabolite availability, which in turn filter microbial colonizers and lead to predictable shifts in composition [2,45,82]. These examples emphasize that host physiology not only responds to microbial cues but also actively sculpts the microbial community landscape, making disentangling cause and effect particularly challenging. At the same time, the relationship is not passive in the other direction; many microbes evolve strategies to override host regulatory processes and manipulate host physiology—particularly sensory systems—in ways that favor their own persistence and transmission.

Some microbes actively manipulate host olfactory cues to enhance their own dissemination. Infected Drosophila, for example, can emit altered odor profiles that attract uninfected individuals, increasing opportunities for horizontal transmission [11,48]. This ability to influence chemical signaling is particularly significant given the central role of chemosensation in locating food, selecting mates, identifying oviposition sites, and avoiding harmful compounds [83,84]. Odorant receptors (ORs) and ionotropic receptors (IRs) detect volatile cues, gustatory receptors (GRs) respond to non-volatile tastants, and odorant-binding proteins (OBPs) transport hydrophobic odor molecules to receptor neurons, collectively forming a sensory network that is susceptible to microbial modulation [85,86].

Evidence for microbial impacts on chemosensory physiology is accumulating across diverse insect taxa. In D. melanogaster, early-life exposure to a natural microbiota enhances adult gustatory decision-making via gut–brain signaling, while antibiotic-treated larvae display reduced odorant chemotaxis that can be restored through microbial recolonization—an effect linked to modulation of GABAergic signaling in the olfactory system [87,88]. In bees, colonization with core gut bacterial species increases sucrose sensitivity and alters brain neurotransmitter levels, with the strongest effects observed in conventionally colonized individuals compared to those with a single-species microbiome [89,90]. In Nasonia giraulti Darling (Hymenoptera: Pteromalidae), Wolbachia infection alters olfactory processing in a manner that increases acceptance of interspecific mates, illustrating how symbionts can shift mate choice through chemosensory pathways [91]. Not all effects are enhancing; in bumble bees, Crithidia bombi Lipa and Triggiani (Kinetoplastea: Trypanosomatidae) infection suppresses responsiveness to sucrose and impairs olfactory discrimination [92], while in honey bees, Deformed Wing Virus reduces sensitivity to floral volatiles such as eucalyptus and peppermint oils [93].

While many of these insights come from controlled laboratory experiments, their ecological significance depends on whether such microbial effects are strong enough to persist amidst environmental variability. Even subtle alterations in chemosensory thresholds can scale into measurable fitness consequences under natural conditions. For example, reductions in sucrose responsiveness caused by C. bombi infections decrease foraging efficiency and pollen collection in bumble bees, impairing colony growth and resilience to stressors such as competition for floral resources and climatic variability [92,94]. In honey bees, microbiome disruptions from pesticides or poor forage diversity increase susceptibility to pathogens and reduce homing accuracy, leaving colonies less fit to cope with nutritional stress or environmental fluctuations [16,95,96]. Conversely, some microbial associations enhance resilience; gut symbionts in mosquitoes can suppress arboviruses [34,97], Wolbachia reduces dengue transmission in the field [98,99], and detoxifying gut bacteria in herbivores can improve survival on chemically defended plants or in pesticide-exposed landscapes [47,100]. Thus, microbial modulation can either exacerbate vulnerability or buffer against environmental challenges, depending on the ecological context. These findings underscore that microbiome effects are not trivial in the wild but instead interact with environmental stressors to shape overall fitness and population dynamics. Such influences are not limited to direct host–microbe interactions; plant-associated microbes can also reshape the chemical landscape insects perceive, altering foraging, oviposition, and trophic interactions.

Microbial influences on chemosensation can be conceptualized as occurring at two levels: direct physiological modulation of insect sensory pathways (e.g., altered receptor expression or neuronal signaling) and indirect ecological modulation, in which microbes reshape the chemical stimuli that sensory systems detect. While the underlying sensory machinery of the insect remains unchanged in the latter case, its functional output is nevertheless modulated because the cues entering olfactory or gustatory pathways are different. Microbial modulation of chemosensation is not limited to direct effects on the insect host; it also occurs indirectly through plant-mediated changes in chemical signaling. Plant-associated microbes can alter volatile organic compound (VOC) profiles, thereby modifying plant attractiveness to insect herbivores, pollinators, or natural enemies [101,102]. Some pathogens exploit this pathway to enhance their spread. For example, infection of maize by the fungus Fusarium verticillioides (Saccardo) Nirenberg (Ascomycota: Nectriaceae) induces emission of volatiles such as acorenol and 1-octen-3-ol, which attract Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) caterpillars that then aid fungal dispersal [103]. Conversely, certain beneficial endophytes induce VOC blends that attract predators or parasitoids of herbivores, effectively recruiting natural enemies into the plant’s defense network [9,104].

Although the capacity of microbes to alter insect chemosensory physiology is now well established, the underlying molecular pathways linking microbial metabolites or immune modulation to changes in receptor expression, neuronal signaling, or behavioral output are unknown. The extent to which environmental variation—such as temperature shifts, pesticide exposure, or habitat disturbance—modulates these interactions is also poorly resolved, as is the relative contribution of olfactory versus gustatory pathways in mediating microbe-induced behavioral changes. Furthermore, few studies have attempted to predictably link microbiome composition to sensory-driven behaviors, limiting the ability to design targeted microbiome-based interventions.

Addressing these knowledge gaps will require integrative approaches that combine metagenomic and transcriptomic profiling with neurophysiological assays and ecological field studies. Such efforts could reveal how specific microbes or microbial consortia alter the sensory circuits underlying foraging, mating, and oviposition behaviors, and how these effects vary across environmental contexts. Elucidating the causal links between microbiome composition, chemosensory physiology, and insect behavior could open the door to novel control strategies that manipulate microbial communities or their chemical signals to disrupt pest behaviors, reduce vector–host contact, or lure insects into traps.

5. Microbiome Effects on Fitness and Vector Competence

Insect-associated microbes can exert substantial and measurable impacts on host reproduction, longevity, and capacity to acquire and transmit pathogens, thereby influencing both ecological dynamics and public health outcomes (Figure 2). While the phenotypic consequences of these associations are well documented—such as Wolbachia-induced cytoplasmic incompatibility [75,76] or microbiome-mediated modulation of mosquito vector competence [34,97,105]—the molecular basis of many of these effects remains incompletely understood. Emerging work is beginning to link microbial metabolites, immune pathways, and host gene expression to these outcomes [3,35,106], but further integrative studies are needed to connect ecological observations with mechanistic detail. Among the most well-studied examples is Wolbachia, a maternally inherited bacterium that manipulates host reproduction through cytoplasmic incompatibility, feminization, male-killing, and parthenogenesis [71,76,107]. These manipulations often bias host populations toward females, enhancing Wolbachia’s vertical transmission. In social insects such as ants, Wolbachia infection has been shown to increase early-life egg production in queens and extend the lifespan of sterile workers, thereby indirectly supporting colony growth and the production of more infected reproductives [108]. In the mosquito Aedes albopictus (Skuse) (Diptera: Culicidae), high Wolbachia densities are associated with reduced dengue virus replication and transmission potential, illustrating its role in modulating vector competence [97].

Other symbionts also influence host reproduction and fitness. Cardinium, another maternally inherited bacterium, can induce feminization [109], parthenogenesis [110], and cytoplasmic incompatibility [111], with some strains increasing fecundity in arthropods such as predatory mites and parasitoid wasps [112,113]. These reproductive alterations not only shape host population structure but also enhance symbiont persistence.

Core, coevolved symbionts often play essential roles in immunity and development. In tsetse flies (Glossina morsitans morsitans Westwood (Diptera: Glossinidae)), the obligate symbiont Wigglesworthia is crucial for immune system maturation, promoting hemocyte differentiation via odorant-binding protein 6 (OBP6)-mediated regulation of the melanization cascade [35]. Conversely, Spiroplasma infections in Glossina fuscipes fuscipes Newstead (Diptera: Glossinidae) can impair reproductive performance by altering sex-biased gene expression and lipid metabolism, reducing sperm motility and competitiveness [114]. These examples underscore that microbiome effects can be beneficial, neutral, or detrimental depending on host–symbiont compatibility and environmental context.

Mosquito gut microbiota represent another critical determinant of vector competence. Distinct gut compartments harbor characteristic microbial assemblages—for example, Tanticharoenia dominates the crop while Elizabethkingia is prevalent in the midgut—each contributing to different metabolic functions, from fermentation to nitrogen cycling [105]. Many gut bacteria encode biosynthetic gene clusters for secondary metabolites such as siderophores, which sequester iron and can inhibit Plasmodium development [34,106]. Experimental manipulation of these communities reveals that germ-free mosquitoes often live longer but exhibit reduced fecundity and diminished capacity to transmit pathogens. Remarkably, supplementation with microbial-derived vitamin B can restore wild-type reproductive and metabolic phenotypes [115]. These vitamins function as essential cofactors in core metabolic pathways, including amino acid and nucleotide biosynthesis, energy metabolism, and methylation reactions, which directly support oogenesis, sperm viability, and overall host fertility [33,115]. Thus, the microbiome’s capacity to supply B vitamins highlights a direct biochemical link between microbial metabolites and insect fitness. Such examples illustrate how seemingly small microbial contributions to host metabolism can scale into colony-level consequences, a dynamic that is particularly evident in pollinators, where stable microbiomes underpin nutrient assimilation, immune regulation, and resilience against pathogens.

Pollinator health also depends on a stable and functional core microbiome. In honeybees (Apis mellifera Linnaeus (Hymenoptera: Apidae)), a small set of core bacterial taxa—including Snodgrassella alvi Olofsson and Vásquez (Betaproteobacteria: Neisseriaceae), Gilliamella apicola Kwong and Moran (Gammaproteobacteria: Orbaceae), Frischella perrara Engel et al. (Gammaproteobacteria: Orbaceae), Lactobacillus, Bifidobacterium, and Commensalibacter—supports nutrient metabolism, immune regulation, and pathogen defense [6,116]. Disruptions to this community from environmental stressors, such as pesticide exposure or poor forage diversity, can shift the relative abundance of these taxa, impairing colony performance and pollination services [16,95]. Given that many crops depend on bee pollination, microbiome disturbances in pollinators have far-reaching implications for agricultural productivity.

Parasitoid wasps, in particular, display microbiome–host interactions with significant implications for development, reproduction, and their effectiveness as biological control agents. In Nasonia spp., for example, the microbiome exhibits phylosymbiosis, with community structure reflecting host phylogeny and contributing to traits relevant to hybrid incompatibility and speciation [117]; for example, Wolbachia in these wasps confers reproductive advantages, and its density must be tightly controlled across generations to avoid deleterious effects on host fitness [118]. Parasitism itself can reshape the microbiome of host insects, whereby caterpillars parasitized by Cotesia spp. undergo profound gut community shifts, frequently involving expansion of Wolbachia, with consequences for both parasitoid larval success and host immunity [119,120,121]. These interactions may extend across trophic levels: parasitism of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) by Cotesia spp. not only altered host gut bacterial composition but also modulated induced defense responses in maize, demonstrating how parasitoid-mediated microbiome changes can influence plant–insect dynamics [122,123]. At the community level, facultative symbionts in aphids, such as Regiella insecticola Moran et al. (Hemiptera: Aphididae: Symbiotobacteriaceae), can reduce or enhance susceptibility to aphidiine parasitoids, thereby shaping parasitoid–host networks in natural populations [124,125,126,127]. Together, these studies underscore that parasitoid performance is contingent on both the wasp’s microbiome and that of its host, highlighting an underexplored dimension of microbiome-informed biological control.

Despite considerable progress, several knowledge gaps limit our ability to harness microbiome manipulation for vector and pest control. First, the fitness effects of many symbionts remain context-dependent and can shift under different environmental conditions or in novel host backgrounds, complicating predictions of their long-term dynamics. Second, the interplay between microbial modulation of immunity and reproductive output is poorly understood, especially in field settings where multiple symbionts and pathogens may interact. Finally, the molecular mechanisms linking specific microbial metabolites to changes in vector competence are only beginning to be unraveled, leaving room for targeted biochemical and genetic studies.

Understanding these interactions has direct applied potential. Symbionts such as Wolbachia are already being deployed in mosquito release programs to suppress arbovirus transmission, while others may be harnessed to impair pathogen development, reduce vector survival, or disrupt reproductive output. Expanding the portfolio of candidate symbionts and elucidating their mechanisms of action could lead to a new generation of microbiome-informed strategies that are environmentally sustainable and evolutionarily robust.

Table 1. Representative examples of insect–microbiome interactions influencing physiology, behavior, and control strategies.

Aspect	Microbial Association	Host Insect(s)	Effect	Ref
Physiology	Core gut bacteria (S. alvi, G. apicola)	Honeybee (A. mellifera)	Enhances digestion, immune regulation, pathogen defense	[6,116]
	H. defensa, APSE phages	Aphids (A. pisum)	Provides resistance to parasitoids through phage-encoded toxins	[54,55]
	Horizontal gene transfer (fungal carotenoid genes, bacterial pectinases)	Aphids (A. pisum), stick insects (Phasmatodea)	Expands pigment production and plant cell-wall digestion capacities	[51,53]
Behavior	Wolbachia infection	Nasonia spp. (parasitoid wasps)	Alters mate choice and reproductive compatibility	[117,118]
	C. bombi infection	Bumblebees (Bombus terrestris (Linnaeus) (Hymenoptera: Apidae))	Reduces sucrose sensitivity and impairs foraging	[92]
	Gut bacteria and microbial volatiles	Drosophila melanogaster, mosquitoes	Modulate olfactory preferences, foraging, and host-seeking	[11,87,88]
Control strategies	Wolbachia releases	Aedes aegypti (Linnaeus) (Diptera: Culicidae), Ae. albopictus	Reduces vector competence for dengue, Zika	[98,99]
	Entomopathogenic nematodes (Steinernematidae, Heterorhabditidae)	Soil- and wood-dwelling insect pests	Rapid host mortality, environmentally safe biocontrol	[128,129]
	Entomopathogenic fungi (Beauveria bassiana (Balsamo-Crivelli) Vuillemin (Ascomycota: Cordycipitaceae), Metarhizium anisopliae (Metschnikoff) Sorokin (Ascomycota: Clavicipitaceae))	Multiple insect pests	Infection through cuticle penetration and immune suppression	[130,131]
	Microbial volatiles in lure-and-kill systems	Lepidoptera, Diptera	Attract or repel insects, enhancing integrated pest management (IPM)	[11,12]

summarizes representative examples of insect–microbiome interactions across physiology, behavior, and control strategies, illustrating the diverse mechanisms through which microbes influence insect biology and the implications for applied management.

6. Environmental and Anthropogenic Disruption

Because many insects acquire a substantial portion of their microbiome through oral ingestion and contact with environmental reservoirs, their microbial communities are inherently sensitive to both abiotic and biotic changes in the surrounding habitat [2,79]. Environmental factors such as soil composition, floral resources, and climate directly influence the diversity and function of environmental microbes, thereby shaping the pool of potential symbionts available for acquisition. Consequently, disturbances to these reservoirs—whether through climate change, land-use modification, or chemical pollution—can have cascading effects on insect health, fitness, and ecological roles.

Agrochemical exposure represents one of the most pervasive anthropogenic pressures on insect microbiomes. Pesticides can directly reduce microbial diversity in insects and in their surrounding environments, altering both core and transient microbial taxa [80,81]. Herbicides such as glyphosate have received particular attention for their capacity to disrupt microbial communities across trophic levels. By inhibiting the shikimate pathway in plants and many microbes, glyphosate shifts plant-associated microbiomes and indirectly modifies the microbial assemblages available to herbivorous insects [132,133]. In pollinators, glyphosate exposure reduces the abundance of key gut bacteria such as S. alvi and G. apicola, impairing digestion, immune regulation, and pathogen resistance [16,96]. In beetles, glyphosate can disrupt vitamin-producing bacterial symbionts, leading to deficiencies in essential micronutrients that impact reproduction and survival [134].

Not all microbial shifts induced by chemicals are detrimental to insects; in some cases, symbionts confer resistance to anthropogenic stressors. For example, Caballeronia symbionts in bean bugs (Riptortus pedestris (Fabricius) (Hemiptera: Alydidae)) can degrade organophosphate insecticides, reducing host susceptibility [47]. Similarly, gut bacteria in the fall armyworm (S. frugiperda) have been shown to metabolize insecticide substrates, contributing to the species’ persistence as a major agricultural pest despite extensive chemical control measures [82,100]. These protective effects, however, raise concerns that anthropogenic pressures may inadvertently select for microbiomes that enhance pest resilience, undermining control strategies.

Landscape-level changes also play a significant role in shaping insect microbiomes. Insects inhabiting forested or semi-natural habitats often harbor more taxonomically diverse and functionally beneficial microbial assemblages than conspecifics in intensively managed agricultural or urban landscapes [135,136]. For bees, landscape context interacts with pathogen pressure to shape gut community composition; bees from more diverse floral landscapes exhibit higher microbial diversity and lower pathogen loads, whereas bees in monoculture-dominated landscapes often exhibit reduced microbiome stability and increased pathogen susceptibility [94,137].

Despite growing evidence that environmental and anthropogenic factors can profoundly alter insect microbiomes, key questions remain unresolved. The resilience and recovery dynamics of microbiomes following disturbance are poorly understood, as is the capacity for beneficial microbiota to be restored through habitat restoration or targeted probiotic supplementation. Moreover, the indirect effects of environmental change on microbiomes via altered plant–microbe–insect interactions remain largely unexplored, particularly for non-pollinator insects and vector species.

Addressing these gaps will be critical for integrating microbiome considerations into pest and pollinator management. Environmental stewardship that preserves or restores microbial reservoirs—such as diversified planting schemes, reduced chemical use, and conservation of natural habitats—could help maintain microbiome integrity, supporting both pest suppression and ecosystem services. In this context, microbiome-informed management strategies can act as a bridge between agricultural productivity, biodiversity conservation, and long-term ecological resilience.

7. Microbe-Based Insect Control

Microbial insecticides—derived from bacteria, fungi, algae, protozoa, or viruses—are increasingly promoted as ecologically sustainable alternatives to synthetic chemical pesticides, offering the potential for specificity, biodegradability, and reduced non-target impacts [129,138]. These biocontrol agents exploit naturally evolved mechanisms of infection, colonization, and mortality induction, providing modes of action that differ from those of conventional insecticides and can help mitigate the development of resistance.

Bacterial agents such as Bacillus thuringiensis Berliner (Firmicutes: Bacillaceae) have long been used in pest management, with crystalline δ-endotoxins that disrupt midgut epithelial integrity following ingestion [139]. Other bacteria, including Pseudomonas protegens Ramette, Frapolli, Défago and Moënne-Loccoz (Gammaproteobacteria: Pseudomonadaceae), exhibit multiple modes of action through the production of secondary metabolites with both insecticidal and antimicrobial properties [140]. Actinobacteria, such as Streptomyces sp. KSF103, have shown multi-stage toxicity against mosquito larvae and adults, offering novel bioactive compounds for vector control [141].

Entomopathogenic fungi such as B. bassiana and M. anisopliae penetrate the insect cuticle via enzymatic degradation, proliferating in the hemocoel and ultimately killing the host through nutrient depletion, toxin production, and immune suppression [130,131]. Advances in formulation technology—such as oil-based carriers and microencapsulation—have improved the persistence and infectivity of fungal agents under variable environmental conditions [142].

Alongside microbial pathogens such as bacteria and fungi, entomopathogenic nematodes (EPNs) of the families Steinernematidae and Heterorhabditidae represent one of the most successful and widely implemented groups of biological control agents against soil-dwelling and wood-boring insect pests. Their efficacy stems from a mutualistic relationship with symbiotic bacteria (e.g., Xenorhabdus spp. and Photorhabdus spp.), which are released into the insect hemocoel following penetration and rapidly produce toxins that kill the host within 24–48 h [128,143]. EPNs possess many attributes of ideal control agents: broad efficacy across diverse pests, minimal non-target effects, compatibility with standard agricultural spraying equipment, and a favorable regulatory status that exempts them, including transgenic strains, from registration requirements in the U.S. and several other countries [128].

Recent work highlights behavioral and population-level considerations. For instance, studies on mosquito-parasitic mermithid nematodes (Romanomermis iyengari Welch (Nematoda: Mermithidae) and Strelkovimermis spiculatus Poinar and Camino (Nematoda: Mermithidae)) demonstrate sophisticated host-selection strategies; infective juveniles can discriminate between uninfected and previously parasitized mosquito larvae, and avoid hosts with high parasite loads, a behavior thought to prevent superparasitism and support long-term host–parasite population stability [144,145]. These findings suggest that, although mermithids differ taxonomically and ecologically from entomopathogenic nematodes, complex behavior governing infection and host regulation may be a broader feature within parasitic nematode groups. Enhancing our understanding of such dynamics could improve field deployment strategies and overall efficacy. Together, the high virulence, safety profile, and behavioral sophistication of EPNs make them a cornerstone of sustainable insect control in integrated pest management programs.

Building on this spectrum of naturally occurring antagonists, viral pathogens—particularly baculoviruses—represent another major group of biological insecticides, valued for their host specificity and capacity for self-dissemination. Viral agents, particularly baculoviruses, have been deployed against lepidopteran pests with high host specificity and self-dissemination potential [146]. Protozoan pathogens, including Nosema spp., can induce chronic infections that impair feeding, reproduction, and longevity in target species [147]. While these agents can establish persistent infections in pest populations, concerns remain over their environmental stability, production costs, and possible sublethal impacts on non-target organisms.

Beyond classical pathogens, the exploitation of microbial metabolites and volatiles offers novel behavioral manipulation strategies. Microbe-derived volatiles can function as attractants in lure-and-kill systems or as repellents to protect crops and stored products [11,12]. Similarly, the deliberate reintroduction of specific microbiota into “sterilized” or microbiome-depleted hosts has been explored to restore beneficial traits or to engineer symbionts that reduce vector competence. For example, genetically modified Wolbachia strains have been developed to block arbovirus replication in Aedes mosquitoes, providing a self-sustaining means of reducing disease transmission [98,99].

However, the adoption of microbial control agents faces significant challenges. Many are sensitive to environmental conditions such as UV radiation, temperature, and humidity, leading to short field persistence and the need for repeated applications [148]. Production and formulation must balance cost, stability, and efficacy while ensuring a narrow host range to minimize harm to beneficial insects, including pollinators and natural enemies. Furthermore, regulatory frameworks and public perception influence the pace of commercialization, particularly for genetically engineered microbes and symbionts.

Future directions will likely integrate microbial agents into multi-tactic IPM programs, leveraging their compatibility with natural enemies, reduced chemical residues, and potential to evolve alongside target pests. Advances in synthetic biology, microbiome engineering, and precision delivery methods are poised to expand the scope and efficiency of microbe-based insect control, while also addressing ecological safety and sustainability.

8. Outlook

The insect microbiome has emerged as a central driver of host physiology, behavior, and ecological interactions, influencing processes as diverse as nutrient assimilation, immune regulation, reproductive strategies, chemosensory perception, and vector competence (Figure 3) [1,3,34,73]. These microbial communities do not function in isolation; they are shaped by an interplay of host genetics, environmental reservoirs, diet, and interspecific interactions, creating feedback loops that extend beyond individual hosts [2,3]. In doing so, they exert influence not only on individual fitness but also on population-level dynamics, trophic networks, and the epidemiology of vector-borne diseases [3,15,22].

Anthropogenic change—including habitat conversion, climate shifts, agricultural intensification, and chemical inputs—has introduced rapid and often destabilizing pressures on insect-associated microbiomes [77,81]. Alterations in microbial diversity and function can cascade into changes in host behavior, pathogen transmission, and crop pollination, with significant implications for both agricultural productivity and public health outcomes [15,16,95]. The dual role of microbes as both beneficial symbionts and potential agents of manipulation highlights the need for nuanced, context-specific understanding of host–microbe–environment interactions [3,79].

Harnessing this knowledge for pest and vector control offers a promising pathway toward sustainable, targeted, and ecologically compatible strategies. Microbiome-based interventions—ranging from probiotic supplementation and microbial volatiles to engineered symbionts and pathogen-blocking endosymbionts—can, in principle, deliver precision control with minimal off-target effects [11,98,99]. Recent work emphasizes the potential of mining insect microbiomes for novel bioactive compounds, biopesticides, and symbiont-mediated RNAi approaches, as well as the promise of paratransgenesis for vector control [10,149]. However, achieving this potential will require closing key knowledge gaps. First, the mechanisms by which microbes modulate chemosensory systems, immunity, and reproductive biology remain incompletely resolved [3,28,89]. Second, the evolutionary stability of introduced or engineered microbial traits under field conditions is uncertain, with potential for unintended ecological consequences or resistance evolution [8,150]. Third, the complex interplay between environmental change and microbiome resilience is poorly understood, limiting predictive power in applied contexts [3,9,16,95].

Future progress will depend on integrative approaches that combine high-resolution multi-omics, behavioral assays, and ecological modeling with controlled field trials. Such efforts should be coupled with rigorous ecological risk assessment frameworks to evaluate persistence, specificity, and potential non-target impacts. Interdisciplinary collaboration—spanning microbiology, chemical ecology, vector biology, agronomy, and policy—will be essential to translate mechanistic insight into scalable, field-ready applications.

Ultimately, the promise of microbiome-informed pest and vector control lies in its potential to align agricultural productivity and public health goals with ecological stewardship. By leveraging naturally occurring or engineered microbial functions, we may be able to design interventions that are not only effective in the short term but also robust to evolutionary and environmental change. Achieving this vision will require both scientific innovation and governance structures capable of supporting safe, adaptive, and evidence-based deployment of microbiome-based strategies.