Ayako Wada-Katsumata

Insects groom their antennae to enhance olfactory acuity

Grooming, a common behavior in animals, serves the important function of removing foreign materials from body surfaces. When antennal grooming was prevented in the American cockroach, Periplaneta americana, field emission gun scanning electron microscopy images revealed that an unstructured substance accumulated on nongroomed antennae, covering sensillar pores, but not on groomed antennae of the same individuals. Gas chromatography analysis of antennal extracts showed that over a 24-h period nongroomed antennae accumulated three to four times more cuticular hydrocarbons than groomed antennae. Moreover, nongroomed antennae accumulated significantly more environmental contaminants from surfaces (stearic acid) and from air (geranyl acetate) than groomed antennae. We hypothesized that the accumulation of excess native cuticular hydrocarbons on the antennae would impair olfactory reception. Electroantennogram experiments and single-sensillum recordings supported this hypothesis: antennae that were prevented from being groomed were significantly less responsive than groomed antennae to the sex pheromone component periplanone-B, as well as to the general odorants geranyl acetate and hexanol. We therefore conclude that antennal grooming removes excess native cuticular lipids and foreign chemicals that physically and/or chemically interfere with olfaction, and thus maintains the olfactory acuity of the antennae. Similar experimental manipulations of the German cockroach (Blattella germanica), carpenter ant (Camponotus pennsylvanicus), and the housefly (Musca domestica), which use different modes of antennal grooming, support the hypothesis that antennal grooming serves a similar function in a wide range of insect taxa.

Gut bacteria mediate aggregation in the German cockroach

Significance There is great interest in elucidating the diverse roles of microbes in biology, in general and, specifically, in mediating animal communication. We demonstrate that the gut bacterial community plays a pivotal role in production of aggregation pheromones in the German cockroach. The feces of normal and gut bacteria-inoculated cockroaches emits highly attractive volatile carboxylic acids (VCAs) that elicit aggregation whereas bacteria-free feces contains few VCAs and is relatively unattractive. VCAs may reflect the gut microbiota and, in turn, the cockroachs local environment, explaining why divergent chemical structures have been proposed as aggregation pheromones. This new insight emphasizes the importance of gut microbes in insect–insect communication and highlights the plasticity of the chemistry and function of fecal aggregation pheromones. Aggregation of the German cockroach, Blattella germanica, is regulated by fecal aggregation agents (pheromones), including volatile carboxylic acids (VCAs). We demonstrate that the gut microbial community contributes to production of these semiochemicals. Chemical analysis of the fecal extract of B. germanica revealed 40 VCAs. Feces from axenic cockroaches (no microorganisms in the alimentary tract) lacked 12 major fecal VCAs, and 24 of the remaining compounds were represented at extremely low amounts. Olfactory and aggregation bioassays demonstrated that nymphs strongly preferred the extract of control feces over the fecal extract of axenic cockroaches. Additionally, nymphs preferred a synthetic blend of 6 fecal VCAs over a solvent control or a previously identified VCA blend. To test whether gut bacteria contribute to the production of fecal aggregation agents, fecal aerobic bacteria were cultured, isolated, and identified. Inoculation of axenic cockroaches with individual bacterial taxa significantly rescued the aggregation response to the fecal extract, and inoculation with a mix of six bacterial isolates was more effective than with single isolates. The results indicate that the commensal gut microbiota contributes to production of VCAs that act as fecal aggregation agents and that cockroaches discriminate among the complex odors that emanate from a diverse microbial community. Our results highlight the pivotal role of gut bacteria in mediating insect–insect communication. Moreover, because the gut microbial community reflects the local environment, local plasticity in fecal aggregation pheromones enables colony-specific odors and fidelity to persistent aggregation sites.

Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica.

SUMMARY In ants, including Formica japonica, trophallaxis and grooming are typical social behaviors shared among nestmates. After depriving ants of either food or nestmates and then providing them with either food or nestmates, a behavioral change in type and frequency of social interactions was observed. We hypothesized that starvation and isolation affected levels of brain biogenic amines including dopamine (DA) and octopamine (OA) – neuromediators modifying various insect behaviors – and tested the relationship between brain biogenic amines and social behaviors of stressed ants. Ants starved for 7 days contained lower brain DA levels and they did not perform trophallaxis toward nestmates. Feeding starved ants sucrose solution re-established trophallaxis but not brain DA levels. The performance of trophallaxis induced recovery of brain DA content to the level of untreated ants. Ants that were isolated for 2 days displayed markedly increased OA levels, which following nestmate interactions, returned to levels similar to those of control (non-isolated) ants and ants isolated for 1 h. We conclude that: (1) starvation reduced brain DA level but had no significant effect on brain OA (trophallaxis recovered the brain DA levels), and (2) isolation increased brain OA level but had no effect on brain DA (trophallaxis and grooming events recovered the brain OA levels). We suggest that social interactions with nestmates influenced brain biogenic amine homeostasis in stressed F. japonica.

Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae)

The exploitation of parental care is common in avian and insect ‘cuckoos’ and these species engage in a coevolutionary arms race. Caterpillars of the lycaenid butterfly Niphanda fusca develop as parasites inside the nests of host ants (Camponotus japonicus) where they grow by feeding on the worker trophallaxis. We hypothesized that N. fusca caterpillars chemically mimic host larvae, or some particular castes of the host ant, so that the caterpillars are accepted and cared for by the host workers. Behaviourally, it was observed that the host workers enthusiastically tended glass dummies coated with the cuticular chemicals of larvae or males and those of N. fusca caterpillars living together. Cuticular chemical analyses revealed that N. fusca caterpillars grown in a host ant nest acquired a colony-specific blend of cuticular hydrocarbons (CHCs). Furthermore, the CHC profiles of the N. fusca caterpillars were particularly close to those of the males rather than those of the host larvae and the others. We suggest that N. fusca caterpillars exploit worker care by matching their cuticular profile to that of the host males, since the males are fed by trophallaxis with workers in their natal nests for approximately ten months.

Hemimetabolous genomes reveal molecular basis of termite eusociality

Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.Eusociality evolved independently in Hymenoptera and in termites. Here, the authors sequence genomes of the German cockroach and a drywood termite and provide insights into the evolutionary signatures of termite eusociality.

Differential Inputs from Chemosensory Appendages Mediate Feeding Responses to Glucose in Wild-Type and Glucose-Averse German Cockroaches, Blattella germanica

Glucose is a universal phagostimulant in many animal species, including the cockroach Blattella germanica. However, some natural populations of B. germanica have been found that are behaviorally deterred from eating glucose. In dose-response studies, glucose was a powerful phagostimulant for wild-type cockroaches, but it strongly deterred feeding in a glucose-averse strain. Both strains, however, exhibited identical dose-response curves to other phagostimulants and deterrents. As a lead to electrophysiological and molecular genetics studies to investigate the mechanisms that underlie glucose-aversion, we used 2 assay paradigms to delineate which chemosensory appendages on the head contribute to the reception of various phagostimulatory and deterrent chemicals. Both simultaneous dual stimulation of the antenna and mouthparts of the insects and 2-choice preference tests in surgically manipulated insects showed that the glucose-averse behavior could be elicited through the gustatory systems of the antennae and mouthparts. The paraglossae alone were sufficient for maximum sensitivity to both phagostimulants and deterrents, including glucose as a deterrent in the glucose-averse strain. In addition to the paraglossae, the labial palps were more important than the maxillary palps in the reception of deterrents (caffeine in both strains and glucose in the glucose-averse strain). The maxillary palps, on the other hand, played a more important role in the reception of phagostimulants (fructose in both strains and glucose in the wild-type strain). Our results suggest that distinct inputs from the chemosensory system mediate opposite feeding responses to glucose in the wild-type and glucose-averse strains.

Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica

Abstract The acquisition of genome sequences from a wide range of insects and other arthropods has revealed a broad positive correlation between the complexity of their chemical ecology and the size of their chemosensory gene repertoire. The German cockroach Blattella germanica is an extreme omnivore and has the largest chemosensory gene repertoire known for an arthropod, exceeding even the highly polyphagous spider mite Tetranychus urticae. While the Odorant Receptor family is not particularly large, with 123 genes potentially encoding 134 receptors (105 intact), the Gustatory Receptor family is greatly expanded to 431 genes potentially encoding 545 receptors (483 intact), the largest known for insects and second only to the spider mite. The Ionotropic Receptor family of olfactory and gustatory receptors is vastly expanded to at least 897 genes (604 intact), the largest size known in arthropods, far surpassing the 150 known from the dampwood termite Zootermopsis nevadensis. Commensurately, the Odorant Binding Protein family is expanded to the largest known for insects at 109 genes (all intact). Comparison with the far more specialized, but phylogenetically related termite, within the Dictyoptera, reveals considerable gene losses from the termite, and massive species‐specific gene expansions in the cockroach. The cockroach has lost function of 11%–41% of these three chemoreceptor gene families to pseudogenization, and most of these are young events, implying rapid turnover of genes along with these major expansions, presumably in response to changes in its chemical ecology.

Persistence of a sugar-rejecting cockroach genotype under various dietary regimes

Glucose-aversion is a heritable trait that evolved in a number of German cockroach (Blattella germanica L.) populations in response to strong selection with glucose-containing insecticide baits. However, in the absence of glucose-containing bait, glucose-averse (GA) cockroaches have lower performance than wild-type (WT) cockroaches in several fitness-determining traits. We allocated 48 caged populations initiated with homozygous GA and WT adults to four dietary treatments consisting of either pure rodent chow, rodent chow mixed to yield a content of either 20% glucose or 20% fructose, or a treatment consisting of choice between the 20% glucose- and the 20% fructose-containing food. After 6 months we found significantly higher frequency of WT individuals in populations restricted to the 20% glucose food, and after 12 months all dietary treatments contained significantly more WT individuals than expected. In accompanying experiments, we found lower survival and longer development time of GA nymphs restricted to glucose-containing food. We furthermore found evidence for assortative mating of females with males from their own genotype, with significant differences within WT cockroaches. Our study shows experimental evidence that within heterogeneous populations, WT German cockroaches will over time prevail in abundance over GA individuals, even when glucose is not a dietary component.

Effectiveness of Boric Acid by Ingestion, But Not by Contact, Against the Common Bed Bug (Hemiptera: Cimicidae)

Boric acid has been used as an insecticide in the successful control of agricultural, public health and urban pests long before the advent of synthetic organic pesticides. Boric acid products, formulated as dusts, sprays, granular baits, pastes, gels, and liquids, are widely available to consumers and pest management professionals, especially to control pest infestations within homes. Boric acid dust is commonly used against bed bugs (Cimex lectularius L. [Hemiptera: Cimicidae]), but its efficacy has not been demonstrated. We evaluated the efficacy of boric acid as an ingestible and residual contact insecticide on bed bugs, and compared its efficacy on the German cockroach (Blattella germanica L. [Blattodea: Ectobiidae]) which is known to be susceptible to boric acid by both routes. Dose-response studies of 0-5% boric acid in blood demonstrated that ingested boric acid caused rapid mortality at concentrations of ≥2%, and even 0.5% and 1% boric acid caused 100% mortality, albeit at a slower time course. In contrast, bed bugs survived contact with high concentrations of boric acid dust. Smaller boric acid particles did not increase mortality of either unfed or recently fed bed bugs. The same boric acid products were effective at causing mortality of German cockroaches by both contact and ingestion. We thus conclude that although boric acid is an excellent candidate active ingredient for an ingestible bait formulation, residual applications of dust or spray would be ineffective in bed bug interventions.

Changes in the Peripheral Chemosensory System Drive Adaptive Shifts in Food Preferences in Insects

A key challenge in understanding the evolution of animal behaviors is to identify cellular and molecular mechanisms that underlie the evolution of adaptive traits and behaviors in polymorphic populations under local selection pressures. Despite recent advances in fish, mice, and insects, there are still only a few compelling examples of major genes and cellular mechanisms associated with complex behavioral changes. Shifts in food or host preferences in insects, accompanied by changes in the peripheral chemosensory system, offer some of the best examples of adaptive behavioral evolution. A remarkable example is the German cockroach, Blattella germanica, a major indoor pest with a highly diverse omnivorous diet. Strong and persistent selection pressure with toxic-baits has induced rapid evolution of behavioral resistance in multiple cockroach populations. While typical cockroaches detect and accept the sugar glucose as a feeding-stimulant, behaviorally resistant cockroaches avoid eating glucose-containing toxic baits by sensing glucose as a deterrent. We review the peripheral gustatory neural mechanisms of glucose-aversion and discuss how the rapid emergence of taste polymorphisms can impede pest control efforts and affect foraging and mate-choice in adapted cockroach populations.