Rapid evolution of chemosensory receptor genes in a pair of sibling species of orchid bees (Apidae: Euglossini).

BackgroundInsects rely more on chemical signals (semiochemicals) than on any other sensory modality to find, identify, and choose mates. In most insects, pheromone production is typically regulated through biosynthetic pathways, whereas pheromone sensory detection is controlled by the olfactory system. Orchid bees are exceptional in that their semiochemicals are not produced metabolically, but instead male bees collect odoriferous compounds (perfumes) from the environment and store them in specialized hind-leg pockets to subsequently expose during courtship display. Thus, the olfactory sensory system of orchid bees simultaneously controls male perfume traits (sender components) and female preferences (receiver components). This functional linkage increases the opportunities for parallel evolution of male traits and female preferences, particularly in response to genetic changes of chemosensory detection (e.g. Odorant Receptor genes). To identify whether shifts in pheromone composition among related lineages of orchid bees are associated with divergence in chemosensory genes of the olfactory periphery, we searched for patterns of divergent selection across the antennal transcriptomes of two recently diverged sibling species Euglossa dilemma and E. viridissima.ResultsWe identified 3185 orthologous genes including 94 chemosensory loci from five different gene families (Odorant Receptors, Ionotropic Receptors, Gustatory Receptors, Odorant Binding Proteins, and Chemosensory Proteins). Our results revealed that orthologs with signatures of divergent selection between E. dilemma and E. viridissima were significantly enriched for chemosensory genes. Notably, elevated signals of divergent selection were almost exclusively observed among chemosensory receptors (i.e. Odorant Receptors).ConclusionsOur results suggest that rapid changes in the chemosensory gene family occurred among closely related species of orchid bees. These findings are consistent with the hypothesis that strong divergent selection acting on chemosensory receptor genes plays an important role in the evolution and diversification of insect pheromone systems

Volatile codes: Correlation of olfactory signals and reception in Drosophila-yeast chemical communication.

Drosophila have evolved strong mutualistic associations with yeast communities that best support their growth and survival, resulting in the development of novel niches. It has been suggested that flies recognize their cognate yeasts primarily based on the rich repertoire of volatile organic compounds (VOCs) derived from the yeasts. Thus, it remained an exciting avenue to study whether fly spp. detect and discriminate yeast strains based on odor alone, and if so, how such resolution is achieved by the olfactory system in flies. We used two fly species known to exploit different niches and harboring different yeasts, D. suzukii (a pest of fresh fruit) and D. melanogaster (a saprophytic fly and a neurogenetic model organism). We initially established the behavioral preference of both fly species to six Drosophila-associated yeasts; then chemically analyzed the VOC profile of each yeast which revealed quantitative and qualitative differences; and finally isolated and identified the physiologically active constituents from yeast VOCs for each drosophilid that potentially define attraction. By employing chemical, behavioral, and electrophysiological analyses, we provide a comprehensive portrait of the olfactory neuroethological correlates underlying fly-yeast coadaptation in two drosophilids with distinct habitats

Antennal transcriptome profiles of anopheline mosquitoes reveal human host olfactory specialization in Anopheles gambiae

BACKGROUND: Two sibling members of the Anopheles gambiae species complex display notable differences in female blood meal preferences. An. gambiae s.s. has a well-documented preference for feeding upon human hosts, whereas An. quadriannulatus feeds on vertebrate/mammalian hosts, with only opportunistic feeding upon humans. Because mosquito host-seeking behaviors are largely driven by the sensory modality of olfaction, we hypothesized that hallmarks of these divergent host seeking phenotypes will be in evidence within the transcriptome profiles of the antennae, the mosquito's principal chemosensory appendage. RESULTS: To test this hypothesis, we have sequenced antennal mRNA of non-bloodfed females from each species and observed a number of distinct quantitative and qualitative differences in their chemosensory gene repertoires. In both species, these gene families show higher rates of sequence polymorphisms than the overall rates in their respective transcriptomes, with potentially important divergences between the two species. Moreover, quantitative differences in odorant receptor transcript abundances have been used to model potential distinctions in volatile odor receptivity between the two sibling species of anophelines. CONCLUSION: This analysis suggests that the anthropophagic behavior of An. gambiae s.s. reflects the differential distribution of olfactory receptors in the antenna, likely resulting from a co-option and refinement of molecular components common to both species. This study improves our understanding of the molecular evolution of chemoreceptors in closely related anophelines and suggests possible mechanisms that underlie the behavioral distinctions in host seeking that, in part, account for the differential vectorial capacity of these mosquitoes

Chemosensory sensitivity reflects reproductive status in the ant Harpegnathos saltator.

Insects communicate with pheromones using sensitive antennal sensilla. Although trace amounts of pheromones can be detected by many insects, context-dependent increased costs of high sensitivity might lead to plasticity in sensillum responsiveness. We have functionally characterized basiconic sensilla of the ant Harpegnathos saltator for responses to general odors in comparison to cuticular hydrocarbons which can act as fertility signals emitted by the principal reproductive(s) of a colony to inhibit reproduction by worker colony members. When released from inhibition workers may become reproductive gamergates. We observed plasticity in olfactory sensitivity after transition to reproductive status with significant reductions in electrophysiological responses to several long-chained cuticular hydrocarbons. Although gamergates lived on average five times longer than non-reproductive workers, the shift to reproductive status rather than age differences matched the pattern of changes in olfactory sensitivity. Decreasing sensillum responsiveness to cuticular hydrocarbons could potentially reduce mutually inhibitory or self-inhibitory effects on gamergate reproduction

Non-synaptic inhibition between grouped neurons in an olfactory circuit.

Diverse sensory organs, including mammalian taste buds and insect chemosensory sensilla, show a marked compartmentalization of receptor cells; however, the functional impact of this organization remains unclear. Here we show that compartmentalized Drosophila olfactory receptor neurons (ORNs) communicate with each other directly. The sustained response of one ORN is inhibited by the transient activation of a neighbouring ORN. Mechanistically, such lateral inhibition does not depend on synapses and is probably mediated by ephaptic coupling. Moreover, lateral inhibition in the periphery can modulate olfactory behaviour. Together, the results show that integration of olfactory information can occur via lateral interactions between ORNs. Inhibition of a sustained response by a transient response may provide a means of encoding salience. Finally, a CO(2)-sensitive ORN in the malaria mosquito Anopheles can also be inhibited by excitation of an adjacent ORN, suggesting a broad occurrence of lateral inhibition in insects and possible applications in insect control

Chemoreceptor Evolution in Hymenoptera and Its Implications for the Evolution of Eusociality.

Eusocial insects, mostly Hymenoptera, have evolved unique colonial lifestyles that rely on the perception of social context mainly through pheromones, and chemoreceptors are hypothesized to have played important adaptive roles in the evolution of sociality. However, because chemoreceptor repertoires have been characterized in few social insects and their solitary relatives, a comprehensive examination of this hypothesis has not been possible. Here, we annotate ∼3,000 odorant and gustatory receptors in recently sequenced Hymenoptera genomes and systematically compare >4,000 chemoreceptors from 13 hymenopterans, representing one solitary lineage (wasps) and three independently evolved eusocial lineages (ants and two bees). We observe a strong general tendency for chemoreceptors to expand in Hymenoptera, whereas the specifics of gene gains/losses are highly diverse between lineages. We also find more frequent positive selection on chemoreceptors in a facultative eusocial bee and in the common ancestor of ants compared with solitary wasps. Our results suggest that the frequent expansions of chemoreceptors have facilitated the transition to eusociality. Divergent expression patterns of odorant receptors between honeybee and ants further indicate differential roles of chemoreceptors in parallel trajectories of social evolution

Activity in the pallial nerve of knobbed (Busycon carica) and channeled (Busycotypus canaliculatum) whelks recorded during exposure of the osphradium to odorant solutions

Adult horseshoe crabs (Limulus polyphemus) are the preferred bait in the U.S. east coast whelk pot fishery, but their harvest is being restricted because of severe population declines in the Chesapeake and Delaware bays. To identify other baits, the activity in the pallial nerve of whelks was determined during exposure of the osphradium to odorant solutions prepared from horseshoe crab eggs, horseshoe crab hemolymph, and hard clam (Mercenaria mercenaria) tissue. All three elicited significant responses; bait based on them may provide an alternative to the use of adult horseshoe crabs, although extensive behavioral testing remains to be done. Channeled whelk did not respond to molecular weight fractions (>3 kDa and <3 kDa) prepared from horseshoe crab egg odorant solutions but did respond when the molecular weight fractions were recombined. Whelks appear to have broadly tuned chemoreceptors and manufactured baits may need to mimic the complex mixture of odorants derived from natural sources

Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore

While mechanisms to detoxify plant produced, anti-herbivore compounds have been associated with plant host use by herbivores, less is known about the role of chemosensory perception in their life histories. This is especially true for generalists, including chelicerate herbivores that evolved herbivory independently from the more studied insect lineages. To shed light on chemosensory perception in a generalist herbivore, we characterized the chemosensory receptors (CRs) of the chelicerate two-spotted spider mite, Tetranychus urticae, an extreme generalist. Strikingly, T. urticae has more CRs than reported in any other arthropod to date. Including pseudogenes, 689 gustatory receptors were identified, as were 136 degenerin/Epithelial Na+ Channels (ENaCs) that have also been implicated as CRs in insects. The genomic distribution of T. urticae gustatory receptors indicates recurring bursts of lineage-specific proliferations, with the extent of receptor clusters reminiscent of those observed in the CR-rich genomes of vertebrates or C. elegans. Although pseudogenization of many gustatory receptors within clusters suggests relaxed selection, a subset of receptors is expressed. Consistent with functions as CRs, the genomic distribution and expression of ENaCs in lineage-specific T. urticae expansions mirrors that observed for gustatory receptors. The expansion of ENaCs in T. urticae to > 3-fold that reported in other animals was unexpected, raising the possibility that ENaCs in T. urticae have been co-opted to fulfill a major role performed by unrelated CRs in other animals. More broadly, our findings suggest an elaborate role for chemosensory perception in generalist herbivores that are of key ecological and agricultural importance

Neuroethology of olfactory-guided behavior and its potential application in the control of harmful insects

Harmful insects include pests of crops and storage goods, and vectors of human and animal diseases. Throughout their history, humans have been fighting them using diverse methods. The fairly recent development of synthetic chemical insecticides promised efficient crop and health protection at a relatively low cost. However, the negative effects of those insecticides on human health and the environment, as well as the development of insect resistance, have been fueling the search for alternative control tools. New and promising alternative methods to fight harmful insects include the manipulation of their behavior using synthetic versions of "semiochemicals", which are natural volatile and non-volatile substances involved in the intra-and/or inter-specific communication between organisms. Synthetic semiochemicals can be used as trap baits to monitor the presence of insects, so that insecticide spraying can be planned rationally (i.e., only when and where insects are actually present). Other methods that use semiochemicals include insect annihilation by mass trapping, attract-and-kill techniques, behavioral disruption, and the use of repellents. In the last decades many investigations focused on the neural bases of insect's responses to semiochemicals. Those studies help understand how the olfactory system detects and processes information about odors, which could lead to the design of efficient control tools, including odor baits, repellents or ways to confound insects. Here we review our current knowledge about the neural mechanisms controlling olfactory responses to semiochemicals in harmful insects. We also discuss how this neuroethology approach can be used to design or improve pest/vector management strategies.Fil: Reisenman, Carolina Esther. University of California at Berkeley; Estados UnidosFil: Lei, Hong. University of Arizona; Estados UnidosFil: Guerenstein, Pablo Gustavo. Provincia de Entre Ríos. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción. Universidad Autónoma de Entre Ríos. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción; Argentina. Universidad Nacional de Entre Ríos. Facultad de Ingeniería; Argentin