Animals have evolved various strategies to hide from or escape predators, one of which is camouflage. This adaptation helps animals blend into their surroundings using specific colors or patterns. However, many predators possess multispectral vision, enabling them to detect different wavelengths of light, which can make camouflage based on visible light ineffective.

Insects face substantial predation pressure from visual predators such as birds, reptiles and other arthropods. Many insects dwell in environments with low light reflectivity, such as leaves, tree bark, or soil, and any light reflection from their bodies could increase their visibility.

In response to these selective pressures, many insects have evolved specialized antireflective structures in their cuticle, wings and eyes. For example, leafhoppers have a unique coating on their cuticle known as the brochosome. Brochosomes are hollow, honeycomb-like spheres with a diameter ranging from 0.2 to 0.6 micrometers. They are produced in the excretory system called the Malpighian tubules and are secreted through the hindgut, where they are applied as a coating to the new cuticle after molting.

Brochosomes consist of lipids and proteins, but their exact composition and role remain unclear. Some researchers believe that brochosomes may serve as a protective barrier or antireflective layer. To investigate the camouflage role of brochosomes, Wu et al. used a combination of imaging and gene and protein analyses to study the brochosome coverage and UV reflectance in 5 to 25-day-old male and female leafhoppers of the Cicadellidae family.

The results indicated that older individuals had fewer brochosomes than younger ones. The experiments also revealed that brochosomes significantly reduced the reflection of ultraviolet light from the surface of leafhoppers by around 30% and diminished the reflectance of visible and infrared light.

Next, Wu et al. conducted predation experiments using jumping spiders known to prey on leafhoppers by analyzing the time of the first attack and the feeding behavior of the spider. The findings showed that jumping spiders preferred to attack older individuals with less brochosome coverage. This suggests that brochosomes are particularly beneficial for younger leafhoppers.

Gene and protein analyses identified four structural brochosome proteins. Experimentally blocking these proteins induced changes to the morphology of the brochosomes and modified the characteristics of the leafhoppers’ cuticle, including an increased diameter and structural deformation of the honeycomb architecture, alongside elevated UV reflectance. Phylogenetic analysis of the corresponding genes revealed that these proteins likely evolved through gene duplication events followed by a gradual accumulation of genetic modifications.

The study of Wu et al. demonstrates that brochosomes serve as an antireflective camouflage coating in leafhoppers to evade visual predators. The unique structure and composition of the lipids and proteins making up the brochosomes appear to be responsible for the antireflective properties of this coating. Further studies will advance our understanding of insect antipredator adaptations and evolutionary mechanisms underlying ecological niche specialization. Furthermore, they may provide biomimetic insights relevant for developing advanced camouflage technologies by emulating biological nanostructures such as brochosomes.

Predation exerts significant selective pressure on the evolution of various species, driving the development of antipredator strategies across the animal kingdom (Galloway et al., 2020; Stevens and Ruxton, 2019). Camouflage is a widely employed strategy, allowing animals to blend into their surroundings by adjusting their coloration and patterns to reduce detection by visual predators (Hughes et al., 2019; Skelhorn and Rowe, 2016). Nevertheless, the presence of predators with multispectral vision, capable of perceiving nonvisible light spectra like infrared and ultraviolet (UV), can compromise traditional color and pattern-based camouflage (Galloway et al., 2020; Jones et al., 2007; Stevens, 2007; Thery and Gomez, 2010), paralleling the challenges of military camouflage under nonvisible light (Xi et al., 2023). Consequently, achieving alignment between an animal’s surface optical characteristics and its surroundings becomes a crucial requirement in visual camouflage strategies.

Insects, one of the most diverse animal groups on earth, contend with intense predation pressure (Cinel et al., 2020; Sheikh et al., 2017). Many of their predators, including birds, reptiles, and predatory arthropods, rely on visual cues, with some possessing highly developed UV vision, where UV light plays a critical role in locating insect prey (Lim and Ben-Yakir, 2020; Stobbe et al., 2009). Furthermore, the natural backgrounds where insects reside, such as leaves, tree bark, and soil, exhibit minimal light reflection (Endler, 1993). Consequently, light reflections originating from an insect’s body significantly elevate its risk of exposure to predators (Tovee, 1995). To counter this challenge, the various nano- and microstructural features of the insect cuticle have excellent antireflective properties that affect insect body coloration, reduce surface light reflection, and aid camouflage (Vukusic and Sambles, 2003; Watson et al., 2017). The first instances of antireflective structures were observed in the compound eyes of moths, the corneas of which are covered by hexagonally arranged protrusions that are approximately 200 nm apart (Bernhard, 1965; Blagodatski et al., 2015; Clapham and Hutley, 1973). Subsequent research has revealed that antireflective structures are widespread on insect body surfaces, primarily found on compound eyes and wings (Blagodatski et al., 2015; Chotard et al., 2022; Ho et al., 2016; Chan et al., 2019; Stavenga et al., 2006). These nano- and microstructures on the cuticular layer are believed to possess antireflective properties, effectively minimizing light reflections from their bodies and thus preventing detection by predators (Blagodatski et al., 2015; Chotard et al., 2022; Ho et al., 2016; Chan et al., 2019; Stavenga et al., 2006).

Leafhoppers (Cicadellidae), one of the largest insect families with over 22,000 species, possess unique extracuticular coating known as brochosome. Brochosomes, typically hollow, honeycomb-like spheres with a diameter ranging from 0.2 to 0.6 µm, are synthesized in the Malpighian tubules, secreted through the hindgut, and applied as a coating on the fresh cuticle following molting (Rakitov, 2000; Rakitov, 2009). Brochosomes primarily comprise lipids and proteins, with protein content ranging from 45% to 75%, but the exact proteins responsible for brochosome formation remain unknown (Li et al., 2022; Rakitov et al., 2018; Yuan et al., 2023). Some have proposed that brochosomes may serve as a protective layer on the leafhopper’s cuticle surface, with a potential role in enhancing the hydrophobicity of their cuticle surface, providing defense against pathogens and predators (Rakitov and Gorb, 2013a; Rakitov, 2009). Apart from these known function of hydrophobicity and the shedding of brochosomes in helping leafhopper escape spider webs, there is currently no definitive biological evidence supporting other hypothesized functions of brochosomes (Lin et al., 2021; Rakitov and Gorb, 2013a; Rakitov and Gorb, 2013b). The camouflage role of leafhopper brochosomes was first hypothesized by Swain, who proposed that these structures reduce optical reflections to avoid predators (Swain, 1936). Subsequent development of bioinspired synthetic analogues has corroborated their antireflective efficacy, with experimental models demonstrating reduced target visibility under simulated predator vision paradigms (Lei et al., 2020; Yang et al., 2017). Recent mechanistic investigations have further elucidated a geometry-dependent antireflective mechanism intrinsic to brochosome architecture (Wang et al., 2024). These findings collectively demonstrate that leafhoppers have evolved a unique antireflection strategy, distinct from conventional insect adaptations, to minimize surface reflectivity. Building upon this foundation, we hypothesize that brochosomes serve as an integumentary camouflage coating, operating through optical signature suppression to enhance crypsis against visual predators and ultimately improve ecological fitness.

In this study, we combined spectrophotometry, electron microscopy, transcriptome analysis, proteome analysis, gene function validation, and leafhopper and jumping spider bioassays to characterize the protein composition and the function of brochosome in leafhopper camouflage. We focused our research on the rice green leafhopper, Nephotettix cincticeps, a well-known agricultural pest with an extensive research history (Hibino, 1996; Wei et al., 2018; Yan et al., 2021). Our results revealed the pronounced effectiveness of brochosome coverage in reducing light reflection on leafhoppers N. cincticeps, especially within the scope of the UV spectrum. By conducting RNAi experiments, we successfully identified four brochosome structural protein for the first time. The suppression of their synthesis induced changes in brochosome morphology, influencing the optical characteristics of the leafhopper’s cuticle surface. Furthermore, our analysis of the evolutionary origin of brochosomes indicates that they likely originated through a process involving duplication–divergence. Our findings support brochosomes as a unique camouflage coating that enables leafhoppers to evade visual predators.

Leafhoppers exhibit a distinctive grooming behavior, resulting in the deposition of a unique extracuticular coating known as brochosome (Rakitov, 2009). However, the precise characteristics and exact adaptive significance of this specialized coating remain largely unknown. Although they are widely believed to confer hydrophobicity, protecting leafhoppers from water and their own excreta (Rakitov and Gorb, 2013a), similar functionalities are attributed to cuticular waxes on the external surfaces of various insects, including leafhoppers (Andersen, 1979; Bello et al., 2022). Consequently, the functionalities of brochosomes may extend beyond this conventional understanding. In this study, we demonstrated that brochosomes exhibit robust antireflective properties, decreasing the reflectance of the leafhopper cuticle surface, particularly in the UV spectral range. This reduction may reduce visibility to visual predators, contributing to the evasion and predation avoidance (Vukusic and Sambles, 2003; Watson et al., 2017). Thus, brochosomes function as a natural camouflage coating on the leafhopper cuticle surface, playing a pivotal role in reducing leafhoppers’ visibility to visual predators and offering a distinct advantage for their survival in predation scenarios as illustrated in Figure 6.

Figure 6

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The present work has elucidated the function of brochosome as a natural antireflective camouflage coating on leafhoppers’ extracuticular, with its coverage directly influencing the antireflective properties of the cuticle surface (Figures 2A–E–4A–G). Previous studies suggested that arthropods employ various nanostructures formed by proteins, lipids, wax, or adhesive substances on their cuticle surfaces to achieve antireflectivity (Silberglied, 1979). These nanostructures, initially identified in the compound eyes of moths, have been subsequently found to be widely distributed on the cuticle surfaces of insects (Bernhard, 1965; Blagodatski et al., 2015; Chotard et al., 2022; Clapham and Hutley, 1973; Ho et al., 2016; Chan et al., 2019; Stavenga et al., 2006). The nano- and microstructures on insect cuticle surfaces generate a gradual change in refractive index near the surface, leading to antireflectivity (Raut et al., 2011). The degree of reflection reduction depends on the shape of these nanostructures, studies in Drosophila melanogaster have confirmed that modifying the morphology of nanostructures in compound eyes directly impacts their optical performance (Kryuchkov et al., 2020). In this study, a thorough examination of the structural protein composition of brochosome, coupled with RNAi-mediated suppression of BSM coding gene expression, yielded brochosomes with regular structure (dsGFP treatment) and structurally abnormal brochosomes (dsBSM treatment) (Figure 4B–E). Subsequent in vitro experiments provided further evidence of the correlation between the normal structure of brochosome and its antireflective performance (Figure 4J and K). This correlation is likely attributed to the fact that the diameter of the hollow pits in brochosome structure (approximately 100 nm) is considerably smaller than most spectral wavelengths (Burks et al., 2023; Rakitov, 2009). As light passes through these small pits, it undergoes diffraction, while light passing through the ridges of brochosome induces scattering. The interference of diffracted and scattered light between different pits and ridges contributes to the observed extinction features in brochosome (Raut et al., 2011). Biomimetic material and mathematical modeling analyses have clarified the relationship between the extinction features of brochosome and the spacing between hollow pits (Banerjee et al., 2023; Lei et al., 2020; Wang et al., 2024; Yang et al., 2017). Therefore, the regular morphology of brochosome is a robust guarantee for its excellent antireflective performance.

Moreover, we noticed a distinct contrast in the antireflective capabilities when applying brochosomes with regular and irregular structures onto different substrates (quartz glass and brown planthopper wings), especially in the UV region (Figure 4J and K). This indicates that the reduction in reflected light is not only related to the structure of brochosome but also to other factors. SEM observations revealed that some brochosome is embedded in the grooves of the leafhopper cuticle surface or brown planthopper wings, which is not observed on the smooth surface of quartz glass (Figure 4B, Figure 4—figure supplement 2). When the wavelength of light is higher than the size of the structure and the surface has a gradient refractive index, light interacts entirely with the rough surface, causing the light to gradually bend (Raut et al., 2011). Combined with the complex structure formed by brochosomes and nanostructures on the cuticle surface, this result in multiple internal reflections of light within these structures, increasing light absorption and significantly enhancing antireflective performance. Furthermore, the aromatic ring structures, conjugated double bonds, and peptide bonds in the proteins of both the cuticle and brochosomes may contribute to the absorption of UV light, providing another potential reason for their antireflective capabilities in the UV spectral region. Therefore, the antireflective performance of brochosome on the insect cuticle surface might be a result of the combined effect of brochosome and cuticular nanostructures.

UV light serves as a crucial visual cue for various insect predators, enhancing foraging, navigation, mating behavior, and prey identification (Cronin and Bok, 2016; Morehouse et al., 2017; Silberglied, 1979). Predators such as birds, reptiles, and predatory arthropods often rely on UV vision to detect prey (Church et al., 1998; Li and Lim, 2005; Zou et al., 2011). However, UV reflectance from insect cuticles can disrupt camouflage, increasing the risk of detection and predation, as natural backgrounds like leaves, bark, and soil typically reflect minimal UV light (Endler, 1993; Li and Lim, 2005; Tovee, 1995). To mitigate this risk, insects often possess antireflective cuticular structures that reduce UV and broad-spectrum light reflectance. This strategy is widespread among insects, including cicadas, dragonflies, and butterflies, and has been shown to decrease predator detection rates (Hooper et al., 2006; Siddique et al., 2015; Zhang et al., 2006). For example, the compound eyes of moths feature hexagonal protuberances that reduce UV reflectance, aiding nocturnal concealment (Blagodatski et al., 2015; Stavenga et al., 2006). In butterflies, UV reflectance from eyespots on wings can attract predators, but reducing UV reflectance or eyespot size can lower predation risk and enhance camouflage (Chen et al., 2023; Lyytinen et al., 2004). Hence, the reflection of UV light from the insect cuticle surface increases the risk of predation by disrupting camouflage (Tovee, 1995). In this study, we utilized the jumping spider P. paykulli to explore the impact of the brochosome coating on the leafhopper’s camouflage against predation. Hunting spiders, such as jumping spiders and wolf spiders, are primary predators of leafhoppers (Liu et al., 2015; Oraze and Grigarick, 1989), and the wavelength of UV light plays a crucial role as a visual cue for jumping spiders in identifying and locating their prey compared to the other wavelengths (Li and Lim, 2005; Zou et al., 2011). Our results revealed that P. paykulli displayed a preference for preying on N. cincticeps with a lower brochosome coverage on their cuticle surface (Figures 2G–J–4H–I). Thus, we hypothesize that the combination of brochosome and leafhopper cuticular microstructures exhibits superior antireflective performance in the UV region, effectively reducing UV reflection from leafhopper bodies and consequently diminishing the predator’s ability to identify them. Additionally, spectral measurement data indicated that the wing reflection spectrum of the brown planthopper (Figure 4J) closely resembled the body spectrum of 25-day-old female N. cincticeps (Figure 2E). It is possible that, in the same living environment, other Hemipteran insects would be more conspicuous to visual predators than leafhoppers. Brochosome coating could provide an advantage for leafhoppers to evade visual predators, thereby enhancing their survival rates in interspecific competition. This adaptation could potentially favor the survival of Cicadellidae in environments with high predation pressure, allowing them to thrive in a wider range of environments. Additionally, within the leafhopper population, the brochosome coverage on the cuticle surface of older individuals was notably lower than that of younger individuals, making elderly leafhoppers more susceptible to be detected and captured by predators (Figure 2F–I, Figure 2—figure supplement 1). This may help eliminate older individuals who have lost their reproductive capacity in the population, thereby ensuring the vitality and reproductive power of the population. Therefore, we consider brochosome, as a form of antireflective camouflage coating on the leafhopper’s cuticle surface, represents a more advanced evolutionary strategy against visual predation.

We successfully identified four proteins essential for the structure of brochosomes for the first time (Figure 3). These BSM-encoded genes exhibit typical orphan gene characteristics, consistent with previous findings (Li et al., 2022; Rakitov et al., 2018; Yuan et al., 2023). Orphan genes originate from processes like de novo evolution, horizontal gene transfer (HGT), and duplication–divergence (Light et al., 2014; Tautz and Domazet-Lošo, 2011). To elucidate the evolutionary origin of the four identified BSM genes, we aligned them with all prokaryotic genomes in NCBI and approximately 1000 arthropod genomes. Interestingly, the homologous genes of these BSM genes were exclusively found in leafhopper genomes in the family Cicadellidae, suggesting that the origin of these BSM genes might not be due to de novo evolution or horizontal gene transfer. Combining the species distribution of the four identified BSM genes (as well as their homology) (Figure 5C), we hypothesize that the BSMs were potentially originated from a process involving duplication–divergence. In this scenario, a new gene would be created through gene duplication or transposition, undergoing fast adaptive evolution and losing similarity to the original gene (Light et al., 2014; Tautz and Domazet-Lošo, 2011). For instance, BSM-4 is widely present in Membracoidea species and also has homologous genes in Clastoptera arizonana of Cereopoidea, indicating that BSM-4 may have a common ancestral gene in Cicadomorpha. The specialization of the distal segment of the Malpighian tubule is a characteristic shared by the three major lineages of the infraorder Cicadomorpha: Cercopoidea (spittle-bugs), Cicadoidea (cicadas), and Membracoidea (leafhoppers and treehoppers) (Rakitov, 2002). Cicadas coat the surface of their burrows with secretions from the Malpighian tubules, spittlebug nymphs have their integuments covered with foam synthesized by the Malpighian tubules, and leafhoppers coat their integuments with brochosomes synthesized by the Malpighian tubules (Chang et al., 2019; Rakitov, 2002). The different demands for secretions from the Malpighian tubules among these insects may be the main reason for the rapid adaptive evolution of BSM genes.

Among Auchenorrhyncha insects, most Cicadellidae (leafhoppers) secrete brochosomes, while many Membracidae (treehoppers) exhibit grooming behavior but lack specialized setae (Rakitov, 1996). Considering that Membracidae are derived from Cicadellidae (Dietrich et al., 2001), the formation of the symbiotic relationship between treehoppers and ants might due to the loss of brochosome synthesis capability. Ants create a protective environment around treehoppers, deterring threats and reducing predation pressure, providing a relatively secure living environment, leading to lower predation pressure compared to leafhoppers (Del Claro and Oliveira, 2000; Nelson and Mooney, 2022). Consequently, the need for the protective disguise represented by brochosomes is likely diminished. We hypothesize that environmental changes drive brochosome evolution, supported by the distribution of BSM-2 and BSM-3 paralogs in Auchenorrhyncha. BSM-3 homologs are widespread in Auchenorrhyncha, while BSM-2 is restricted to brochosome-secreting Cicadellidae and absent in most Membracidae. The high structural homology between BSM-2 and BSM-3, despite low sequence similarity, suggests that BSM-2 arose from BSM-3 duplication. We propose that gene duplication/loss events are the primary factors underlying differences in brochosome synthesis between Cicadellidae and Membracidae. Gene duplication/loss is a common mechanism for functional gain/loss in eukaryotes, promoting protein diversity and redundancy (Wong and Belov, 2012). Thus, gene duplication may be a key driver of brochosome formation and functional diversity in leafhoppers.

In summary, our research has underscored the indispensable role of brochosomes as an essential antireflective camouflage coating for leafhoppers, conferring a significant advantage in evading visually oriented predators. We have identified four key BSM encoding genes, a groundbreaking discovery in brochosome research, which suggests that gene duplication may be involved in the formation of these adaptive structures. Our study not only deepens our understanding of leafhoppers' antipredator strategies but also sheds light on the distinct evolutionary trajectories employed by these insects within their ecological niche. This contributes to the development of biomimicry and the advancement of state-of-the-art camouflage technologies. Furthermore, while our study has provided valuable insights into the structure and function of brochosomes, there are still gaps in our knowledge regarding the evolutionary origins of BSMs. Future research should aim to fill these gaps as a more comprehensive understanding of BSMs and their role in brochosome formation will enhance our appreciation of the complex evolutionary processes that have shaped these unique structures. Additionally, the analysis of BSMs in a broader range of leafhopper species will help elucidate the relationship between BSM composition and the morphological and functional diversity of brochosomes, further informing our understanding of the ecological and evolutionary dynamics of this insect group.

All the data needed to understand and assess the conclusions of this research are available in the article, Supplementary Materials, and GenBank (accession number PP273097, PP273098, PP273099, PP273100). Any additional information required to reanalyse the data reported in this paper is available from the lead contact upon request.

1. 1. Wu W

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   ID PP273097. Nephotettix cincticeps brochosomin-1 (BSM-1) mRNA, complete cds.

   https://www.ncbi.nlm.nih.gov/nuccore/PP273097.1/
2. 1. Wu W

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   https://www.ncbi.nlm.nih.gov/nuccore/PP273098.1/
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   https://www.ncbi.nlm.nih.gov/nuccore/PP273099.1/
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   https://www.ncbi.nlm.nih.gov/nuccore/PP273100.1/

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Author details

1. Wei Wu

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Conceptualization, Data curation, Investigation, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   wuwei_19861115@163.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5440-345X

2. Qianzhuo Mao

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Conceptualization, Visualization

   Competing interests

   No competing interests declared

3. Zhuang-Xin Ye

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Data curation, Software

   Competing interests

   No competing interests declared

4. Zhenfeng Liao

   State Key Laboratory for Sustainable Control of Pest and Disease, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, China

   Contribution

   Visualization

   Competing interests

   No competing interests declared

5. Hong-Wei Shan

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Writing – original draft

   Competing interests

   No competing interests declared

6. Jun-Min Li

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

7. Chuan-Xi Zhang

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

8. Jian-Ping Chen

   State Key Laboratory of Agricultural Products Safety, Key Laboratory of Biotechnology in Plant Protection of MARA, Zhejiang Key Laboratory of Green Plant Protection, Institute of Plant Virology, Ningbo University, Ningbo, China

   Contribution

   Conceptualization, Funding acquisition, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   jianpingchen@nbu.edu.cn

   Competing interests

   No competing interests declared

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