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Attine ants engage in a quadripartite symbiosis with fungi they cultivate for food, specialized garden parasites, and parasite-inhibiting bacteria. Molecular phylogenetic evidence supports an ancient host-pathogen association between the ant-cultivar mutualism and the garden parasite. Here we show that ants rear the antibiotic-producing bacteria in elaborate cuticular crypts, supported by unique exocrine glands, and that these structures have been highly modified across the ants' evolutionary history. This specialized structural evolution, together with the absence of these bacteria and modifications in other ant genera that do not grow fungus, indicate that the bacteria have an ancient and coevolved association with the ants, their fungal cultivar, and the garden parasite.

Plant diseases and insect pest damage cause tremendous losses in forestry and fruit tree production. Even though chemical pesticides have been effective in the control of plant diseases and insect pests for several decades, they are increasingly becoming undesirable due to their toxic residues that affect human life, animals, and the environment, as well as the growing challenge of pesticide resistance. In this study, we review the potential of hydrolytic enzymes from Bacillus species such as chitinases, β-1,3-glucanases, proteases, lipases, amylases, and cellulases in the biological control of phytopathogens and insect pests, which could be a more sustainable alternative to chemical pesticides. This study highlights the application potential of the hydrolytic enzymes from different Bacillus sp. as effective biocontrol alternatives against phytopathogens/insect pests through the degradation of cell wall/insect cuticles, which are mainly composed of structural polysaccharides like chitins, β-glucans, glycoproteins, and lipids. This study demonstrates the prospects for applying hydrolytic enzymes from Bacillus sp. as effective biopesticides in forest and fruit tree production, their mode of biocidal activity and dual antimicrobial/insecticidal potential, which indicates a great prospect for the simultaneous biocontrol of pests/diseases. Further research should focus on optimizing the production of hydrolytic enzymes, and the antimicrobial/insecticidal synergism of different Bacillus sp. which could facilitate the simultaneous biocontrol of pests and diseases in forest and fruit tree production.

During each molting cycle of insect development, synthesis of new cuticle occurs concurrently with the partial degradation of the overlying old exoskeleton. Protection of the newly synthesized cuticle from molting fluid enzymes has long been attributed to the presence of an impermeable envelope layer that was thought to serve as a physical barrier, preventing molting fluid enzymes from accessing the new cuticle and thereby ensuring selective degradation of only the old one. In this study, using the red flour beetle, Tribolium castaneum, as a model insect species, we show that an entirely different and unexpected mechanism accounts for the selective action of chitinases and possibly other molting enzymes. The molting fluid enzyme chitinase, which degrades the matrix polysaccharide chitin, is not excluded from the newly synthesized cuticle as previously assumed. Instead, the new cuticle is protected from chitinase action by the T. castaneum Knickkopf (TcKnk) protein. TcKnk colocalizes with chitin in the new cuticle and organizes it into laminae. Down-regulation of TcKnk results in chitinase-dependent loss of chitin, severe molting defects, and lethality at all developmental stages. The conservation of Knickkopf across insect, crustacean, and nematode taxa suggests that its critical roles in the laminar ordering and protection of exoskeletal chitin may be common to all chitinous invertebrates.

Insect cuticle is critical for the environmental adaptability and insecticide resistance of insects. However, there is no clear understanding of the structure and protein components of the cuticle during each developmental stage of holometabolous insects, and knowledge about the protein components within each layer is vague. We conducted serial sectioning, cuticular structure analysis, and transcriptome sequencing of the larval, pupal, and adult cuticles of Bombyx mori. The deposition processes of epicuticle, exocuticle, and endocuticle during larval, pupal, and adult cuticle formation were similar. Transcriptome analysis showed that these cuticle formations share 74% of the expressed cuticular protein (CP) genes and 20 other structural protein genes, such as larval serum protein and prisilkin. There are seven, six, and eleven stage-specific expressed CP genes in larval, pupal, and adult cuticles, respectively. The types and levels of CP genes may be the key determinants of the properties of each cuticular layer. For example, the CPs of the RR-2 protein family with high contents of histidine (His) are more essential for the exocuticle. Functional analysis suggested that BmorCPAP1-H is involved in cuticle formation. This study not only offers an in-depth understanding of cuticle morphology and protein components but also facilitates the elucidation of molecular mechanisms underlying cuticle formation in future studies.

Organisms from temperate zones are exposed to seasonal changes and must be able to cope with a wide range of climatic conditions. Especially ectotherms, including insects, are at risk to desiccate under dry and warm conditions, the more so given the changing climate. To adjust to current conditions, organisms acclimate through changes in physiology, morphology and/or behaviour. Insects protect themselves against desiccation through a layer of cuticular hydrocarbons (CHC) on their body surface. Hence, acclimation may also affect the CHC profile, changing their waterproofing capacity under different climatic conditions. Here, we investigated the acclimation response of two Temnothorax ant species to different climatic conditions. We analysed CHC profiles of queens, nurses and foragers that were acclimated to different humidity × temperature regimes, and tested the beneficial acclimation hypothesis by measuring survival of workers under desiccation‐heat stress. Both ants possessed a species‐specific CHC profile. Nevertheless, they showed similar acclimation responses concerning changes of certain CHC classes, and finally similar survival rates under desiccation‐heat stress. Warm‐acclimated individuals generally showed longer n‐alkanes, fewer dimethyl alkanes, and more (workers) or less (queens) monomethyl alkanes. In contrast, dry conditions resulted in more n‐alkanes and fewer mono‐ and dimethyl alkanes, but these acclimatory changes were only observed in workers and not in queens. Warm‐ and dry‐acclimated workers survived desiccation‐heat stress better, but we found no species differences. Our results indicate that both ant species can plastically adjust their cuticular hydrocarbon profile, allowing them to acclimate to different climatic conditions. Although their CHC composition differs in a species‐specific manner, they showed similar chemical adjustments and concomitant changes in survival rate. Hence, chemical plasticity may be critical to determine a species’ climatic range and its survival under changing climatic conditions. A plain language summary is available for this article. Plain Language Summary

Why does a single fire ant Solenopsis invicta struggle in water, whereas a group can float effortlessly for days? We use time-lapse photography to investigate how fire ants S. invicta link their bodies together to build waterproof rafts. Although water repellency in nature has been previously viewed as a static material property of plant leaves and insect cuticles, we here demonstrate a self-assembled hydrophobic surface. We find that ants can considerably enhance their water repellency by linking their bodies together, a process analogous to the weaving of a waterproof fabric. We present a model for the rate of raft construction based on observations of ant trajectories atop the raft. Central to the construction process is the trapping of ants at the raft edge by their neighbors, suggesting that some \"cooperative\" behaviors may rely upon coercion.

The functional characterization of an entire class of 17 genes from the red flour beetle, Tribolium castaneum , which encode two families of C uticular P roteins A nalogous to P eritrophins (CPAPs) has been carried out. CPAP genes in T. castaneum are expressed exclusively in cuticle-forming tissues and have been classified into two families, CPAP1 and CPAP3 , based on whether the proteins contain either one (CPAP1), or three copies (CPAP3) of the chitin-binding domain, ChtBD2, with its six characteristically spaced cysteine residues. Individual members of the TcCPAP1 and TcCPAP3 gene families have distinct developmental patterns of expression. Many of these proteins serve essential and non-redundant functions in maintaining the structural integrity of the cuticle in different parts of the insect anatomy. Three genes of the TcCPAP1 family and five genes of the TcCPAP3 family are essential for insect development, molting, cuticle integrity, proper locomotion or fecundity. RNA interference (RNAi) targeting TcCPAP1-C, TcCPAP1-H, TcCPAP1-J or TcCPAP3-C transcripts resulted in death at the pharate adult stage of development. RNAi for Tc C PAP3-A1, TcCPAP3-B, TcCPAP3-D1 or TcCPAP3-D2 genes resulted in different developmental defects, including adult/embryonic mortality, abnormal elytra or hindwings, or an abnormal ‘stiff-jointed’ gait. These results provide experimental support for specialization in the functions of CPAP proteins in T. castaneum and a biological rationale for the conservation of CPAP orthologs in other orders of insects. This is the first comprehensive functional analysis of an entire class of cuticular proteins with one or more ChtBD2 domains in any insect species.

AIM : In ectotherms, the colour of an individual’s cuticle may have important thermoregulatory and protective consequences. In cool environments, ectotherms should be darker, to maximize heat gain, and larger, to minimize heat loss. Dark colours should also predominate under high UV-B conditions because melanin offers protection. We test these predictions in ants (Hymenoptera: Formicidae) across space and through time based on a new, spatially and temporally explicit, global-scale combination of assemblage-level and environmental data. LOCATION : Africa, Australia and South America. METHODS : We sampled ant assemblages (n5274) along 14 elevational transects on three continents. Individual assemblages ranged from 250 to 3000 m a.s.l. (minimum to maximum range in summer temperature of 0.5–35 8C). We used mixed-effects models to explain variation in assemblage cuticle lightness. Explanatory variables were average assemblage body size, temperature and UVB irradiation. Annual temporal changes in lightness were examined for a subset of the data. RESULTS : Assemblages with large average body sizes were darker in colour than those with small body sizes. Assemblages became lighter in colour with increasing temperature, but darkened again at the highest temperatures when there were high levels of UV-B. Through time, temperature and body size explained variation in lightness. Both the spatial and temporal models explained c. 50% of the variation in lightness. MAIN CONCLUSIONS : Our results are consistent with the thermal melanism hypothesis, and demonstrate the importance of considering body size and UVB radiation exposure in explaining the colour of insect cuticle. Crucially, this finding is at the assemblage level. Consequently, the relative abundances and identities of ant species that are present in an assemblage can change in accordance with environmental conditions over elevation, latitude and relatively short time spans. These findings suggest that there are important constraints on how ectotherm assemblages may be able to respond to rapidly changing environmental conditions.

This review covers selected literature from 1982 to the present on some of the ecological, behavioral, and biochemical aspects of hydrocarbon use by insects and other arthropods. Major ecological and behavioral topics are species- and gender-recognition, nestmate recognition, task-specific cues, dominance and fertility cues, chemical mimicry, and primer pheromones. Major biochemical topics include chain length regulation, mechanism of hydrocarbon formation, timing of hydrocarbon synthesis and transport, and biosynthesis of volatile hydrocarbon pheromones of Lepidoptera and Coleoptera. In addition, a section is devoted to future research needs in this rapidly growing area of science.

Entomopathogenic fungi and their insect hosts represent a model system for examining invertebrate-pathogen coevolutionary selection processes. Here we report the characterization of competing components of an arms race consisting of insect protective antimicrobial compounds and evolving fungal mechanisms of detoxification. The insect pathogenic fungus Beauveria bassiana has a remarkably wide host range; however, some insects are resistant to fungal infection. Among resistant insects is the tenebrionid beetle Tribolium castaneum that produces benzoquinone-containing defensive secretions. Reduced fungal germination and growth was seen in media containing T. castaneum dichloromethane extracts or synthetic benzoquinone. In response to benzoquinone exposure, the fungus expresses a 1,4-benzoquinone oxidoreductase, BbbqrA , induced >40-fold. Gene knockout mutants ( ΔBbbqrA ) showed increased growth inhibition, whereas B. bassiana overexpressing BbbqrA ( Bb::BbbqrA ᴼ) displayed increased resistance to benzoquinone compared with wild type. Increased benzoquinone reductase activity was detected in wild-type cells exposed to benzoquinone and in the overexpression strain. Heterologous expression and purification of BbBqrA in Escherichia coli confirmed NAD(P)H-dependent benzoquinone reductase activity. The ΔBbbqrA strain showed decreased virulence toward T. castaneum , whereas overexpression of BbbqrA increased mortality versus T. castaneum . No change in virulence was seen for the ΔBbbqrA or Bb::BbbqrA ᴼ strains when tested against the greater wax moth Galleria mellonella or the beetle Sitophilus oryzae , neither of which produce significant amounts of cuticular quinones. The observation that artificial overexpression of BbbqrA results in increased virulence only toward quinone-secreting insects implies the lack of strong selection or current failure of B. bassiana to counteradapt to this particular host defense throughout evolution. Although entomopathogenic fungi and their invertebrate hosts share a >300 million year co-evolutionary history, little is known concerning the biochemical and genetic basis of insect defensive tactics and the countermeasures evolved and evolving by the pathogen to thwart these defenses. Our results provide a molecular mechanism to help explain why some insects are more resistant to broad host-range entomopathogenic fungi. We identify beetle cuticular secretions and a fungal detoxifying enzyme as components of an arms race between insects and the fungal pathogen, suggesting an evolving role for the quinone reductase enzyme as a specific virulence factor for host quinone detoxification. As races have winners and losers, this paper captures a snapshot where the host is leading the race.