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Bacterial intracellular symbiosis (endosymbiosis) is widespread in nature and impacts many biological processes. In holometabolous symbiotic insects, metamorphosis entails a complete and abrupt internal reorganization that creates a constraint for endosymbiont transmission from larvae to adults. To assess how endosymbiosis copes—and potentially evolves—throughout this major host-tissue reorganization, we used the association between the cereal weevil Sitophilus oryzae and the bacterium Sodalis pierantonius as a model system. S. pierantonius are contained inside specialized host cells, the bacteriocytes, that group into an organ, the bacteriome. Cereal weevils require metabolic inputs from their endosymbiont, particularly during adult cuticle synthesis, when endosymbiont load increases dramatically. By combining dual RNA-sequencing analyses and cell imaging, we show that the larval bacteriome dissociates at the onset of metamorphosis and releases bacteriocytes that undergo endosymbiosis-dependent transcriptomic changes affecting cell motility, cell adhesion, and cytoskeleton organization. Remarkably, bacteriocytes turn into spindle cells and migrate along the midgut epithelium, thereby conveying endosymbionts to midgut sites where future mesenteric caeca will develop. Concomitantly, endosymbiont genes encoding a type III secretion system and a flagellum apparatus are transiently up-regulated while endosymbionts infect putative stem cells and enter their nuclei. Infected cells then turn into new differentiated bacteriocytes and form multiple new bacteriomes in adults. These findings show that endosymbiosis reorganization in a holometabolous insect relies on a synchronized host–symbiont molecular and cellular “choreography” and illustrates an adaptive feature that promotes bacteriome multiplication to match increased metabolic requirements in emerging adults.

Background The insect gut microbiota has been shown to contribute to the host’s digestion, detoxification, development, pathogen resistance, and physiology. However, there is poor information about the ranking of these roles. Most of these results were obtained with cultivable bacteria, whereas the bacterial physiology may be different between free-living and midgut-colonizing bacteria. In this study, we provided both proteomic and genomic evidence on the ranking of the roles of gut bacteria by investigating the anal droplets from a weevil, Cryptorhynchus lapathi . Results The gut lumen and the anal droplets showed qualitatively and quantitatively different subsets of bacterial communities. The results of 16S rRNA sequencing showed that the gut lumen is dominated by Proteobacteria and Bacteroidetes, whereas the anal droplets are dominated by Proteobacteria. From the anal droplets, enzymes involved in 31 basic roles that belong to 7 super roles were identified by Q-TOF MS. The cooperation between the weevil and its gut bacteria was determined by reconstructing community pathway maps, which are defined in this study. A score was used to rank the gut bacterial roles. The results from the proteomic data indicate that the most dominant role of gut bacteria is amino acid biosynthesis, followed by protein digestion, energy metabolism, vitamin biosynthesis, lipid digestion, plant secondary metabolite (PSM) degradation, and carbohydrate digestion, while the order from the genomic data is amino acid biosynthesis, vitamin biosynthesis, lipid digestion, energy metabolism, protein digestion, PSM degradation, and carbohydrate digestion. The PCA results showed that the gut bacteria form functional groups from the point of view of either the basic role or super role, and the MFA results showed that there are functional variations among gut bacteria. In addition, the variations between the proteomic and genomic data, analyzed with the HMFA method from the point of view of either the bacterial community or individual bacterial species, are presented. Conclusion The most dominant role of gut bacteria is essential nutrient provisioning, followed by digestion and detoxification. The weevil plays a pioneering role in diet digestion and mainly digests macromolecules into smaller molecules which are then mainly digested by gut bacteria.

The recent Californian hot drought (2012–2016) precipitated unprecedented ponderosa pine ( Pinus ponderosa ) mortality, largely attributable to the western pine beetle ( Dendroctonus brevicomis ; WPB). Broad-scale climate conditions can directly shape tree mortality patterns, but mortality rates respond non-linearly to climate when local-scale forest characteristics influence the behavior of tree-killing bark beetles (e.g., WPB). To test for these cross-scale interactions, we conduct aerial drone surveys at 32 sites along a gradient of climatic water deficit (CWD) spanning 350 km of latitude and 1000 m of elevation in WPB-impacted Sierra Nevada forests. We map, measure, and classify over 450,000 trees within 9 km 2 , validating measurements with coincident field plots. We find greater size, proportion, and density of ponderosa pine (the WPB host) increase host mortality rates, as does greater CWD. Critically, we find a CWD/host size interaction such that larger trees amplify host mortality rates in hot/dry sites. Management strategies for climate change adaptation should consider how bark beetle disturbances can depend on cross-scale interactions, which challenge our ability to predict and understand patterns of tree mortality. The 2012–2016 drought and western pine beetle outbreaks caused unprecedented mortality of ponderosa pine in the Sierra Nevada, California. Here, the authors analyse drone-based data from almost half a million trees and find an interaction between host size and climatic water deficit, with higher mortality for large trees in dry, warm conditions but not in cooler or wetter conditions.

When insects harm plants, they activate relevant enzyme systems for defense, and changes in enzyme activity, to a certain extent, reflect the host plant’s ability to resist insect damage. Alfalfa leaf weevils ( Hypera postica Gyllenhal) are the main economic insect pest of alfalfa, which seriously affect its yield and quality. To clarify the effects of feeding induction by alfalfa leaf weevil larvae and adults on defense enzymes in alfalfa, ‘Zhongmu No. 1’ variety was used as the experimental material. Comprehensive correlation analysis and principal component analysis were used to evaluate the corresponding patterns of 12 physiological indicators of alfalfa induced by insect feeding of different densities. Results showed that after feeding induction by adult and larval alfalfa leaf weevils, total antioxidant capacity (T-AOC), malondialdehyde (MDA), phenylalanine ammonia-lyase (PAL), tyrosine ammonia lyase (TAL), lipoxygenase (LOX), chymotrypsin inhibitors (CI), trypsin inhibitor (TI), and jasmonic acid (JA) in the alfalfa leaves increased with increasing feeding time. However, activities of catalase (CAT), peroxidase (POD), superoxide dismutase (SOD) and polyphenolic oxidase (PPO) in alfalfa leaves first increased and then decreased, showing a downward trend.

Thousands of species of ambrosia beetles excavate tunnels in wood to farm fungi. They maintain associations with particular lineages of fungi, but the phylogenetic extent and mechanisms of fidelity are unknown. We test the hypothesis that selectivity of their mycangium enforces fidelity at coarse phylogenetic scales, while permitting promiscuity among closely related fungal mutualists. We confirm a single evolutionary origin of the Xylosandrus complex—a group of several xyleborine genera that farm fungi in the genus Ambrosiella . Multi-level co-phylogenetic analysis revealed frequent symbiont switching within major Ambrosiella clades, but not between clades. The loss of the mycangium in Diuncus , a genus of evolutionary cheaters, was commensurate with the loss of fidelity to fungal clades, supporting the hypothesis that the mycangium reinforces fidelity. Finally, in vivo experiments tracked symbiotic compatibility throughout the symbiotic life cycle of Xylosandrus compactus and demonstrated that closely related Ambrosiella symbionts are interchangeable, but the probability of fungal uptake in the mycangium was significantly lower in more phylogenetically distant species of symbionts. Symbiont loads in experimental subjects were similar to wild-caught beetles. We conclude that partner choice in ambrosia beetles is achieved in the mycangium, and co-phylogenetic inferences can be used to predict the likelihood of specific symbiont switches.

Scientific cinematography using ultrafast optical imaging is a common tool to study motion. In opaque organisms or structures, X-ray radiography captures sequences of 2D projections to visualize morphological dynamics, but for many applications full four-dimensional (4D) spatiotemporal information is highly desirable. We introduce in vivo X-ray cine-tomography as a 4D imaging technique developed to study real-time dynamics in small living organisms with micrometer spatial resolution and sub-second time resolution. The method enables insights into the physiology of small animals by tracking the 4D morphological dynamics of minute anatomical features as demonstrated in this work by the analysis of fast-moving screw-and-nut—type weevil hip joints. The presented method can be applied to a broad range of biological specimens and biotechnological processes.

Eucryptorrhynchus scrobiculatus (Motschulsky) and E. brandti (Harold) are 2 serious pests inflicting damage on Ailanthus altissima (Mill.) Swingle. In the field, these species exhibit aggregation behavior.We hypothesized that this behavior facilitated the contact and horizontal transfer of Metarhizium anisopliae (Metschn.) Sorokin in weevil species. Little or no mortality in both E. scrobiculatus and E. brandti adult individuals exposed to low concentrations M. anisopliae (1 × 105, 1 × 106 conidia/ml). A mortality rate of 100% was observed in both E. scrobiculatus and E. brandti adults after 3 and 5 d of treatment with M. anisopliae at concentrations of 1 × 109 and 1 × 108 conidia/ml.The aggregation behavior of E. scrobiculatus and E. brandti adults was unaffected by M. anisopliae. In the transfer test of M. anisopliae, the mortality rate of recipients mixed with donors treated with M. anisopliae conidia was significantly higher compared to untreated donors and control recipients in laboratory and field experiments. Furthermore, the mortality of secondary recipients in both E. scrobiculatus and E. brandti was significantly higher than that of the control group.The findings suggested that horizontal transfer of M. anisopliae occurred in both species, which was further supported by microscopy observation and the activity of immune-related enzymes in the donor, recipient, and secondary recipient. Our findings demonstrated a specific method for improving pest control by combining aggregation behavior with the use of biopesticides, thereby enhancing the understanding of biological management strategies. Graphical Abstract The adults were transferred to another Petri dish as donors and were mixed with untreated adults after being treated with M. anisopliae SW23, or purified water (control). The untreated adults who received the mixing treatment were frozen to death, and then they were transferred to a new Petri dish and mixed with other untreated adults.The adults were then used as secondary recipients in the experiments.The different colored dots represent E. scrobiculatus or E. brandti under different treatments in the figure.

Cascading speciation is predicted to occur when multiple interacting species diverge in parallel as a result of divergence in one species promoting adaptive differentiation in other species. However, there are few examples where ecological interactions among taxa have been shown to result in speciation that cascades across multiple trophic levels. Here, we test for cascading speciation occurring among the western pine beetle ( Dendroctonus brevicomis ), its primary host tree ( Pinus ponderosa ), and the beetle's fungal mutualists ( Ceratocystiopsis brevicomi and Entomocorticium sp. B). We assembled genomes for the beetle and a fungal symbiont and then generated reduced representation genomic data (RADseq) from range-wide samples of these three interacting species. Combined with published data for the host tree, we present clear evidence that the tree, the beetle, and the fungal symbionts are all genetically structured into at least two distinct groups that have strongly codiverged with geographical isolation. We then combine our genomic results with diverse population and laboratory-based data to show evidence for reproductive isolation at each level of the cascade and for coevolution of both antagonistic and mutualistic species interactions within this complex network.

The landscape plant, Cinnamomum camphora, is a broad-spectrum insect-repelling tree species, mainly due to a diversity of terpenoids, such as camphor. Despite its formidable chemical defenses, C. camphora is easily attacked and invaded by a monophagous weevil pest, Pagiophloeus tsushimanus. Deciphering the key olfactory signal components regulating host preference could facilitate monitoring and control strategies for this pest. Herein, two host volatiles, camphor and ocimene, induced GC-EAD/EAG reactions in both male and female adult antennae. Correspondingly, Y-tube olfactometer assays showed that the two compounds were attractive to both male and female adults. In field assays, a self-made trap device baited with 5 mg dose d(+)-camphor captured significantly more P. tsushimanus adults than isopropanol solvent controls without sexual bias. The trunk gluing trap device baited with bait can capture adults, but the number was significantly less than that of the self-made trap device and adults often fell after struggling. The cross baffle trap device never trapped adults. Neither ocimene nor isopropanol solvent control captured adults. When used in combination, ocimene did not enhance the attraction of d(+)-camphor to both female and male adults. These results indicate that d(+)-camphor is a key active compound of P. tsushimanus adults for host location. The combination of the host-volatile lure based on d(+)-camphor and the self-made trapping device is promising to monitor and provide an eco-friendly control strategy for this novel pest P. tsushimanus in C. camphora plantations.

A variety of photonic mechanisms give rise to iridescence and other structural colors in insects. In weevils (Coleoptera: Curculionoidea), iridescence is created by the most complex of these mechanisms, the three-dimensional photonic crystal. These self-assembling crystals take the form of triply periodic networks with single diamond or single gyroid symmetries and have been the subject of many descriptive studies based on individual species (often on a single specimen). To determine how these extraordinary nanostructures have evolved, we conduct the first comparative study of photonic crystals and setal nanostructure across Curculionoidea. By integrating structural data with newly available phylogenetic information, we demonstrate that—despite their widespread geographical and taxonomic distribution—three-dimensional photonic crystals appear to have evolved only once in weevils, in the common ancestor of a clade comprising the current subfamilies Entiminae and Cyclominae. Flattened, hollow setae with an unordered, spongy network in the lumen appear to be a necessary precursor to three-dimensional photonic crystals; we propose an evolutionary pathway by which this transformation has occurred.