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Taxon-restricted genes make up a considerable proportion of genomes, yet their contribution to phenotypic evolution is poorly understood. We combined gene expression with functional and behavioral assays to study the origin and adaptive value of an evolutionary innovation exclusive to the water strider genus Rhagovelia: the propelling fan. We discovered that two taxon-restricted genes, which we named geisha and mother-of-geisha, specifically control fan development. geisha originated through a duplication event at the base of the Rhagovelia lineage, and both duplicates acquired a novel expression in a specific cell population prefiguring fan development. These gene duplicates played a central role in Rhagovelia’s adaptation to a new physical environment, demonstrating that the evolution of taxon-restricted genes can contribute directly to evolutionary novelties that allow access to unexploited ecological niches.

Development of insecticide resistance has been a serious concern worldwide, whose mechanisms have been attributed to evolutionary changes in pest insect genomes such as alteration of drug target sites, up-regulation of degrading enzymes, and enhancement of drug excretion. Here, we report a previously unknown mechanism of insecticide resistance: Infection with an insecticide-degrading bacterial symbiont immediately establishes insecticide resistance in pest insects. The bean bug Riptortus pedestris and allied stinkbugs harbor mutualistic gut symbiotic bacteria of the genus Burkholderia, which are acquired by nymphal insects from environmental soil every generation. In agricultural fields, fenitrothion-degrading Burkolderia strains are present at very low densities. We demonstrated that the fenitrothion-degrading Burkholderia strains establish a specific and beneficial symbiosis with the stinkbugs and confer a resistance of the host insects against fenitrothion. Experimental applications of fenitrothion to field soils drastically enriched fenitrothion-degrading bacteria from undetectable levels to >80% of total culturable bacterial counts in the field soils, and >90% of stinkbugs reared with the enriched soil established symbiosis with fenitrothion-degrading BURKHOLDERIA: In a Japanese island where fenitrothion has been constantly applied to sugarcane fields, we identified a stinkbug population wherein the insects live on sugarcane and ≈8% of them host fenitrothion-degrading BURKHOLDERIA: Our finding suggests the possibility that the symbiont-mediated insecticide resistance may develop even in the absence of pest insects, quickly establish within a single insect generation, and potentially move around horizontally between different pest insects and other organisms.

Global warming impacts diverse organisms not only directly but also indirectly via other organisms with which they interact. Recently, the possibility that elevated temperatures resulting from global warming may substantially affect biodiversity through disrupting mutualistic/parasitic associations has been highlighted. Here we report an experimental demonstration that global warming can affect a pest insect via suppression of its obligate bacterial symbiont. The southern green stinkbug Nezara viridula depends on a specific gut bacterium for its normal growth and survival. When the insects were reared inside or outside a simulated warming incubator wherein temperature was controlled at 2.5°C higher than outside, the insects reared in the incubator exhibited severe fitness defects (i.e., retarded growth, reduced size, yellowish body color, etc.) and significant reduction of symbiont population, particularly in the midsummer season, whereas the insects reared outside did not. Rearing at 30°C or 32.5°C resulted in similar defective phenotypes of the insects, whereas no adult insects emerged at 35°C. Notably, experimental symbiont suppression by an antibiotic treatment also induced similar defective phenotypes of the insects, indicating that the host’s defective phenotypes are attributable not to the heat stress itself but to the suppression of the symbiont population induced by elevated temperature. These results strongly suggest that high temperature in the midsummer season negatively affects the insects not directly but indirectly via the heat-vulnerable obligate bacterial symbiont, which highlights the practical relevance of mutualism collapse in this warming world. IMPORTANCE Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula , the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the “Achilles’ heel” of symbiont-dependent organisms under climate change conditions. Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula , the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the “Achilles’ heel” of symbiont-dependent organisms under climate change conditions.

Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major force driving the diversification of phytophagous insects. Although symbiotic bacteria are known to have essential nutritional roles for insects, examples of radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts to diversify into the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria ( Coriobacterium and Gordonibacter ), as well as Firmicutes ( Clostridium ) and Proteobacteria ( Klebsiella ) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota, the Pyrrhocoridae phylogeny is neither congruent with a dendrogram based on the hosts’ microbial community profiles nor phylogenies of individual symbiont strains, indicating frequent horizontal exchange of symbiotic partners. Phylogenetic dating analyses based on the fossil record reveal an origin of the Pyrrhocoridae core microbiota in the late Cretaceous (81.2–86.5 million years ago), following the transition from crypt-associated beta-proteobacterial symbionts to an anaerobic community localized in the M3 region of the midgut. The change in symbiotic syndromes (that is, symbiont identity and localization) and the acquisition of the pyrrhocorid core microbiota followed the evolution of their preferred host plants (Malvales), suggesting that the symbionts facilitated their hosts’ adaptation to this imbalanced nutritional resource and enabled the subsequent diversification in a competition-poor ecological niche.

Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24–40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia’s in vitro thermal optima did not predict in vivo outcomes. Regardless, strain- and temperature- dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.

Insecticide resistance is one of the most serious problems in contemporary agriculture and public health. Although recent studies revealed that insect gut symbionts contribute to resistance, the symbiont-mediated detoxification process remains unclear. Here we report the in vivo detoxification process of an organophosphorus insecticide, fenitrothion, in the bean bug Riptortus pedestris . Using transcriptomics and reverse genetics, we reveal that gut symbiotic bacteria degrade this insecticide through a horizontally acquired insecticide-degrading enzyme into the non-insecticidal but bactericidal compound 3-methyl-4-nitrophenol, which is subsequently excreted by the host insect. This integrated “host-symbiont reciprocal detoxification relay” enables the simultaneous maintenance of symbiosis and efficient insecticide degradation. We also find that the symbiont-mediated detoxification process is analogous to the insect genome-encoded fenitrothion detoxification system present in other insects. Our findings highlight the capacity of symbiosis, combined with horizontal gene transfer in the environment, as a powerful strategy for an insect to instantly eliminate a toxic chemical compound, which could play a critical role in the human-pest arms race. Insect acquisition of insecticide resistance represents a serious problem for agriculture. Here, authors reveal an insect symbiotic bacteria that degrades insecticide fenitrothion into a non-insecticidal but bactericidal compound, which is subsequently excreted by the insect host.

The Pleidae, or pygmy backswimmers, is a family of aquatic bugs (Hemiptera, Heteroptera, Nepomorpha) containing four genera. Here, we describe Plea cryptica sp. nov. and redescribe its sister species, Plea minutissima Leach, 1817. Whereas the morphological distinction of these closely related species is only possible for males, molecular data clearly separate them. As part of our taxonomic study, we provide comprehensive molecular data including more than 200 DNA barcodes from all over Europe, complete nuclear ribosomal DNA, full mitochondrial genome data, and 3D scans for both species. Furthermore, the same molecular markers are also presented for Neoplea striola (Fieber, 1844). We used Maximum Likelihood (ML) analyses to reconstruct the phylogeny of the Pleidae and Notonectoidea based on available mitogenomic data. Our study represents a successful implementation of the proposed concept of taxonomics, using data from high-throughput sequencing technologies for integrative taxonomic studies, and allowing high confidence for both biodiversity and ecological research.

The genus Coridius Illiger, 1807 (Heteroptera: Dinidoridae) comprises a group of phytophagous terrestrial bugs consisting of 36 species distributed in the Afrotropical and Indo-Malayan regions. In several communities in northeastern India, insects are recognised as a delicacy, medicine, and a nutritional supplement, with Coridius being a popular delicacy. However, Coridius has received little taxonomic attention to date due to large intraspecific variations, inadequate taxonomic treatments, and the rarity of many species. To address this gap, an integrative taxonomy of the genus was performed. Two mitochondrial genes, viz., cytochrome oxidase subunit 1 (COI) and 16S rRNA, were sequenced to reconstruct the phylogenetic relationships within Coridius . We performed both maximum likelihood (ML) and Bayesian inference (BI) to develop a species tree, followed by the Bayesian implementation of the Poisson tree process (bPTP) and Assemble Species by Automatic Partitioning (ASAP) as an additional test to assess species boundaries and delimit operational taxonomic units. A linear discriminant analysis (LDA) of four key morphological characters was then performed to identify species groups. Overall, our analysis supported the establishment of three new species: Coridius adii sp. nov., Coridius esculentus sp. nov., and Coridius insperatus sp. nov., and revealed six distinct lineages within Coridius chinensis (Dallas, 1851). Linear discriminant analysis of morphological characters indicated the clustering of eight species. The species status of Coridius nigriventris (Westwood, 1837) stat. rev , formerly synonymized under Coridius nepalensis (Westwood, 1837), is reinstated in this study. Further, we revised the genus Coridius from India and rediscovered Coridius assamensis (Distant, 1902) and Coridius fuscus (Westwood, 1837) after 100 years.

The phenomenon of flower visiting (anthophily) and the pollination, though becoming prevalent with the rise of flowering angiosperms, hypothesized to have originated from the antagonistic relationship of florivory between insects and gymnosperms in the Upper Jurassic. Though not commonly known, this behaviour has been documented in several instances among the representatives of the suborder Heteroptera, i.e., the true bugs. Here, we describe Shaykayatcoris michalskii gen. nov., sp. nov., the first known representative of the plesiomorphic flat bug (Aradidae) subfamily Prosympiestinae in the Upper Cretaceous Burma Terrane amber fauna (Lowermost Cenomanian, ca. 99 Mya). Besides expanding the knowledge on the heteropteran insect fauna of the Lagerstätte, the discovery of this new true bug provides intriguing insights into the evolutionary history of true bugs. First, the new record corroborates that the subfamily Prosympiestinae is a Gondwanan relict group among the representatives of flat bugs. Second, this insect presents the first known incidence of iridescent colouration in flat bugs with a tentative role of camouflage, suggesting a more exposed lifestyle compared to the apomorphic lineages of flat bugs, which have adapted to live under tree bark. Third, the iridescence and the high amount of pollen among the syninclusions suggest that the insect was likely to be anthophilous. The suspected presence of anthophily in such a specialised heteropteran insect group like Aradidae suggests that anthophily was more widespread among the Mesosoic true bugs than it can be observed in the case of extant taxa.

Despite the demonstrated functional importance of gut microbes, our understanding of how animals regulate their metabolism in response to nutritionally beneficial symbionts remains limited. Here, we elucidate the functional importance of the African cotton stainer's (Dysdercus fasciatus) association with two actinobacterial gut symbionts and subsequently examine the insect's transcriptional response following symbiont elimination. In line with bioassays demonstrating the symbionts' contribution towards host fitness through the supplementation of B vitamins, comparative transcriptomic analyses of genes involved in import and processing of B vitamins revealed an upregulation of gene expression in aposymbiotic (symbiont-free) compared with symbiotic individuals; an expression pattern that is indicative of B vitamin deficiency in animals. Normal expression levels of these genes, however, can be restored by either artificial supplementation of B vitamins into the insect's diet or reinfection with the actinobacterial symbionts. Furthermore, the functional characterization of the differentially expressed thiamine transporter 2 through heterologous expression in Xenopus laevis oocytes confirms its role in cellular uptake of vitamin B1. These findings demonstrate that despite an extracellular localization, beneficial gut microbes can be integral to the host's metabolic homeostasis, reminiscent of bacteriome-localized intracellular mutualists.