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1.  Novel Set-Up for Low-Disturbance Sampling of Volatile and Non-volatile Compounds from Plant Roots 
Journal of Chemical Ecology  2015;41(3):253-266.
Most studies on rhizosphere chemicals are carried out in substrate-free set-ups or in artificial substrates using sampling methods that require an air flow and may thus cause disturbance to the rhizosphere. Our study aimed to develop a simplified and inexpensive system that allows analysis of rhizosphere chemicals at experimentally less disturbed conditions. We designed a mesocosm in which volatile rhizosphere chemicals were sampled passively (by diffusion) without air- and water flow on polydimethylsiloxane-(PDMS) tubes. Dandelion (Taraxacum sect. ruderalia) was used as model plant; roots were left undamaged. Fifteen volatiles were retrieved from the sorptive material by thermal desorption for analysis by gas chromatography/mass spectrometry (GC/MS). Furthermore, three sugars were collected from the rhizosphere substrate by aqueous extraction and derivatized prior to GC/MS analysis. In order to study how the quantity of detected rhizosphere compounds depends on the type of soil or substrate, we determined the matrix-dependent recovery of synthetic rhizosphere chemicals. Furthermore, we compared sorption of volatiles on PDMS tubes with and without direct contact to the substrate. The results show that the newly designed mesocosm is suitable for low-invasive extraction of volatile and non-volatile compounds from rhizospheres. We further highlight how strongly the type of substrate and contact of PDMS tubes to the substrate affect the detectability of compounds from rhizospheres.
PMCID: PMC4408369  PMID: 25795090
Root exudates; Gas chromatography/mass spectrometry; Root volatiles; Sugars; Soil substrates
2.  Olfactory Specialization in Drosophila suzukii Supports an Ecological Shift in Host Preference from Rotten to Fresh Fruit 
Journal of Chemical Ecology  2015;41(2):121-128.
It has been demonstrated that Drosophila suzukii is capable of attacking ripening fruit, making it a unique species within a fly family named for their attraction towards the fermentation products associated with rotten fruits, vinegar, and yeast. It also has been hypothesized that D. suzukii is more attracted to the volatiles associated with the earlier ripening stages of fruit development, and in turn, that D. suzukii is less attracted to fermented food resources, especially when compared with D. melanogaster. Here, we demonstrate that D. suzukii and its close relative D. biarmipes are in fact more sensitive to volatiles associated with the fruit-ripening process; however, in choice-assays, both spotted-wing species are more attracted to fermented fruit than to earlier stages of fruit development, which is similar to the behavioral preferences of D. melanogaster, and thus, fruit developmental stage alone does not explain the ecological niche observed for D. suzukii. In contrast, we show that both D. suzukii and D. biarmipes are more attracted to leaf odors than D. melanogaster in behavioral trials. For D. suzukii, this differential behavioral preference towards leaves appears to be linked to β-cyclocitral, a volatile isoprenoid that we show is most likely a novel ligand for the “ab3A” neuron. In addition, this compound is not detected by either of the other two tested fly species.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-015-0544-3) contains supplementary material, which is available to authorized users.
PMCID: PMC4351439  PMID: 25618323
Olfaction; Chemical ecology; Neuroethology; Specialization; Drosophila; Insect behavior
3.  Anatomical and functional analysis of domestication effects on the olfactory system of the silkmoth Bombyx mori 
The silkmoth Bombyx mori is the main producer of silk worldwide and has furthermore become a model organism in biological research, especially concerning chemical communication. However, the impact domestication might have had on the silkmoth's olfactory sense has not yet been investigated. Here, we show that the pheromone detection system in B. mori males when compared with their wild ancestors Bombyx mandarina seems to have been preserved, while the perception of environmental odorants in both sexes of domesticated silkmoths has been degraded. In females, this physiological impairment was mirrored by a clear reduction in olfactory sensillum numbers. Neurophysiological experiments with hybrids between wild and domesticated silkmoths suggest that the female W sex chromosome, so far known to have the sole function of determining femaleness, might be involved in the detection of environmental odorants. Moreover, the coding of odorants in the brain, which is usually similar among closely related moths, differs strikingly between B. mori and B. mandarina females. These results indicate that domestication has had a strong impact on odour detection and processing in the olfactory model species B. mori.
PMCID: PMC3843842  PMID: 24258720
domestication; Bombyx mori; Bombyx mandarina; olfactory sensilla; olfactory coding; W chromosome
4.  Central projections of antennular chemosensory and mechanosensory afferents in the brain of the terrestrial hermit crab (Coenobita clypeatus; Coenobitidae, Anomura) 
The Coenobitidae (Decapoda, Anomura, Paguroidea) is a taxon of hermit crabs that includes two genera with a fully terrestrial life style as adults. Previous studies have shown that Coenobitidae have evolved a sense of spatial odor localization that is behaviorally highly relevant. Here, we examined the central olfactory pathway of these animals by analyzing central projections of the antennular nerve of Coenobita clypeatus, combining backfilling of the nerve with dextran-coupled dye, Golgi impregnations and three-dimensional reconstruction of the primary olfactory center, the antennular lobe. The principal pattern of putative olfactory sensory afferents in C. clypeatus is in many aspects similar to what have been established for aquatic decapod crustaceans, such as the spiny lobster Panulirus argus. However, there are also obvious differences that may, or may not represent adaptations related to a terrestrial lifestyle. In C. clypeatus, the antennular lobe dominates the deutocerebrum, having more than one thousand allantoid-shaped subunits. We observed two distinct patterns of sensory neuron innervation: putative olfactory afferents from the aesthetascs either supply the cap/subcap region of the subunits or they extend through its full depth. Our data also demonstrate that any one sensory axon can supply input to several subunits. Putative chemosensory (non-aesthetasc) and mechanosensory axons represent a different pathway and innervate the lateral and median antennular neuropils. Hence, we suggest that the chemosensory input in C. clypeatus might be represented via a dual pathway: aesthetascs target the antennular lobe, and bimodal sensilla target the lateral antennular neuropil and median antennular neuropil. The present data is compared to related findings in other decapod crustaceans.
PMCID: PMC4502362
chemical ecology; terrestrialization; olfaction; hermit crabs; retrograde tracing
5.  Decoding odor quality and intensity in the Drosophila brain 
eLife  null;3:e04147.
To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.
eLife digest
Organisms need to sense and adapt to their environment in order to survive. Senses such as vision and smell allow an organism to absorb information about the external environment and translate it into a meaningful internal image. This internal image helps the organism to remember incidents and act accordingly when they encounter similar situations again. A typical example is when organisms are repeatedly attracted to odors that are essential for survival, such as food and pheromones, and are repulsed by odors that threaten survival.
Strutz et al. addressed how attractiveness or repulsiveness of a smell, and also the strength of a smell, are processed by a part of the olfactory system called the lateral horn in fruit flies. This involved mapping the neuronal patterns that were generated in the lateral horn when a fly was exposed to particular odors.
Strutz et al. found that a subset of neurons called inhibitory projection neurons processes information about whether the odor is attractive or repulsive, and that a second subset of these neurons process information about the intensity of the odor. Other insects, such as honey bees and hawk moths, have olfactory systems with a similar architecture and might also employ a similar spatial approach to encode information regarding the intensity and identity of odors. Locusts, on the other hand, employ a temporal approach to encoding information about odors.
The work of Strutz et al. shows that certain qualities of odors are contained in a spatial map in a specific brain region of the fly. This opens up the question of how the information in this spatial map influences decisions made by the fly.
PMCID: PMC4270039  PMID: 25512254
olfaction; neural circuit; lateral horn; antennal lobe; odor processing; functional imaging; D. melanogaster
6.  Dopamine drives Drosophila sechellia adaptation to its toxic host 
eLife  null;3:e03785.
Many insect species are host-obligate specialists. The evolutionary mechanism driving the adaptation of a species to a toxic host is, however, intriguing. We analyzed the tight association of Drosophila sechellia to its sole host, the fruit of Morinda citrifolia, which is toxic to other members of the melanogaster species group. Molecular polymorphisms in the dopamine regulatory protein Catsup cause infertility in D. sechellia due to maternal arrest of oogenesis. In its natural host, the fruit compensates for the impaired maternal dopamine metabolism with the precursor l-DOPA, resuming oogenesis and stimulating egg production. l-DOPA present in morinda additionally increases the size of D. sechellia eggs, what in turn enhances early fitness. We argue that the need of l-DOPA for successful reproduction has driven D. sechellia to become an M. citrifolia obligate specialist. This study illustrates how an insect's dopaminergic system can sustain ecological adaptations by modulating ontogenesis and development.
eLife digest
Many insect species rely on another animal or plant species for their own reproduction. For example, a fruit fly called Drosophila sechellia—which is found in the Seychelles—will only feed and lay its eggs on the fruit of a species of tree called Morinda citrifolia. This pairing is particularly unusual because these fruits, commonly called morinda, are toxic to all other Drosophila species.
Female Drosophila sechellia flies produce fewer eggs than other Drosophila species, which makes it difficult to raise this species in the laboratory. However providing these flies with morinda fruit, or chemicals from this fruit, was known to increase the expression of many genes involved in egg production and stimulate the flies to lay more eggs. Nevertheless, the reasons why this species of fruit fly depends on the toxic morinda fruit were unclear.
Now Lavista-Llanos et al. have confirmed that feeding Drosophila sechellia flies a diet of morinda fruit—instead of a typical laboratory diet—causes these flies to produce six-times as many eggs. Furthermore, this morinda diet had effects that went beyond the previously reported stimulatory effects of acidic chemicals in the fruits triggering the flies to lay more eggs.
Egg production in flies is controlled by dopamine, and a lack of this hormone is known to reduce the size of other fruit flies' ovaries and the number of eggs that they produce. Lavista-Llanos et al. went on to feed female Drosophila sechellia flies the chemical building blocks that make up the dopamine hormone, and one such chemical (called l-DOPA) caused the flies to produce more eggs. This did not occur when the flies were fed dopamine itself.
Lavista-Llanos et al. discovered that Drosophila sechellia flies have very high levels of dopamine but much lower levels of l-DOPA than other Drosophila fly species; and revealed that this was because a gene called Catsup is mutated in Drosophila sechellia. When Lavista-Llanos et al. mutated the same gene in another Drosophila species, the mutant flies produced fewer eggs and abnormally accumulated an enzyme (which makes l-DOPA) inside their developing eggs—just like Drosophila sechellia.
The presence of l-DOPA in morinda fruit partly compensates for the reduced fertility of Drosophila sechellia and the other flies with mutations in the Catsup gene. Lavista-Llanos et al. discovered that removing or replacing l-DOPA in the morinda fruit caused the flies to produce fewer eggs. Furthermore, the l-DOPA present in morinda increases the size of Drosophila sechellia eggs, which in turn helps them to survive their toxic environment.
Lavista-Llanos et al. also discovered that feeding dopamine to vulnerable Drosophila species helps them to cope with the toxic effects of a morinda diet. One of the next challenges will be to uncover how chemicals from the morinda fruit affect the dopamine system of the flies. It is also unknown if the dopamine hormone also influences the strong attraction that Drosophila sechellia feels towards its only host, the morinda fruit.
PMCID: PMC4270095  PMID: 25487989
Drosophila sechellia; Morinda citrifolia; dopamine; oogenesis; evolution; tyrosine hydroxilase; D. melanogaster; other
7.  Love makes smell blind: mating suppresses pheromone attraction in Drosophila females via Or65a olfactory neurons 
Scientific Reports  2014;4:7119.
In Drosophila, the male sex pheromone cis-vaccenyl acetate (cVA) elicits aggregation and courtship, through the odorant receptor Or67d. Long-lasting exposure to cVA suppresses male courtship, via a second channel, Or65a. In females, the role of Or65a has not been studied. We show that, shortly after mating, Drosophila females are no longer attracted to cVA and that activation of olfactory sensory neurons (OSNs) expressing Or65a generates this behavioral switch: when silencing Or65a, mated females remain responsive to cVA. Neurons expressing Or67d converge into the DA1 glomerulus in the antennal lobe, where they synapse onto projection neurons (PNs), that connect to higher neural circuits generating the attraction response to cVA. Functional imaging of these PNs shows that the DA1 glomerulus is inhibited by simultaneous activation of Or65a OSNs, which leads to a suppression of the attraction response to cVA. The behavioral role of postmating cVA exposure is substantiated by the observation that matings with starved males, which produce less cVA, do not alter the female response. Moreover, exposure to synthetic cVA abolishes attraction and decreases sexual receptivity in unmated females. Taken together, Or65a mediates an aversive effect of cVA and may accordingly regulate remating, through concurrent behavioral modulation in males and females.
PMCID: PMC4236738  PMID: 25406576
9.  Morphology and Histochemistry of the Aesthetasc-Associated Epidermal Glands in Terrestrial Hermit Crabs of the Genus Coenobita (Decapoda: Paguroidea) 
PLoS ONE  2014;9(5):e96430.
Crustaceans have successfully adapted to a variety of environments including fresh- and saltwater as well as land. Transition from an aquatic to a terrestrial lifestyle required adaptations of the sensory equipment of an animal, particularly in olfaction, where the stimulus itself changes from hydrophilic to mainly hydrophobic, air-borne molecules. Hermit crabs Coenobita spp. (Anomura, Coenobitidae) have adapted to a fully terrestrial lifestyle as adults and have been shown to rely on olfaction in order to detect distant food items. We observed that the specialized olfactory sensilla in Coenobita, named aesthetascs, are immersed in a layer of mucous-like substance. We hypothesized that the mucous is produced by antennal glands and affects functioning of the aesthetascs.
Using various microscopic and histochemical techniques we proved that the mucous is produced by aesthetasc-associated epidermal glands, which we consider to be modified rosette-type aesthetasc tegumental glands known from aquatic decapods. These epidermal glands in Coenobita are multicellular exocrine organs of the recto-canal type with tubulo-acinar arrangement of the secretory cells. Two distinct populations of secretory cells were clearly distinguishable with light and electron microscopy. At least part of the secretory cells contains specific enzymes, CUB-serine proteases, which are likely to be secreted on the surface of the aesthetasc pad and take part in antimicrobial defense. Proteomic analysis of the glandular tissue corroborates the idea that the secretions of the aesthetasc-associated epidermal glands are involved in immune responses.
We propose that the mucous covering the aesthetascs in Coenobita takes part in antimicrobial defense and at the same time provides the moisture essential for odor perception in terrestrial hermit crabs. We conclude that the morphological modifications of the aesthetasc-associated epidermal glands as well as the functional characteristics of their secretions are important adaptations to a terrestrial lifestyle.
PMCID: PMC4013018  PMID: 24805352
10.  Evolution of insect olfactory receptors 
eLife  2014;3:e02115.
The olfactory sense detects a plethora of behaviorally relevant odor molecules; gene families involved in olfaction exhibit high diversity in different animal phyla. Insects detect volatile molecules using olfactory (OR) or ionotropic receptors (IR) and in some cases gustatory receptors (GRs). While IRs are expressed in olfactory organs across Protostomia, ORs have been hypothesized to be an adaptation to a terrestrial insect lifestyle. We investigated the olfactory system of the primary wingless bristletail Lepismachilis y-signata (Archaeognatha), the firebrat Thermobia domestica (Zygentoma) and the neopteran leaf insect Phyllium siccifolium (Phasmatodea). ORs and the olfactory coreceptor (Orco) are with very high probability lacking in Lepismachilis; in Thermobia we have identified three Orco candidates, and in Phyllium a fully developed OR/Orco-based system. We suggest that ORs did not arise as an adaptation to a terrestrial lifestyle, but evolved later in insect evolution, with Orco being present before the appearance of ORs.
eLife digest
Detecting chemical cues can be a matter of life or death for insects, and many employ three families of receptor proteins to detect a broad range of odors. Members of one of these receptor families, the olfactory receptors, form a complex with another protein, the olfactory coreceptor that is essential for both positioning and stabilizing the receptor, as well as the actual function.
Crustaceans share a common ancestor with insects, and since they do not have olfactory receptors it has been proposed that these receptors evolved when prehistoric insects moved from the sea to live on land. According to this idea, olfactory receptors evolved because these ancestors needed to be able to detect odor molecules floating in the air rather than dissolved in water.
Previous research on insect olfactory receptors has focused on insects with wings. Missbach et al. have now used a wide range of techniques to investigate how evolutionarily older wingless insect groups detect scents. As all investigated groups evolved from a common ancestor at different times these experiments allow tracking of the historical development of olfactory receptors.
In the wingless species that is more closely related to the flying insects there was evidence of the presence of multiple coreceptors but not the olfactory receptors themselves. In the most basal insects no evidence for any part of the olfactory receptor-based system was found. This indicates that the main olfactory receptors evolved independently of the coreceptor long after the migration of insects from water to land. Missbach et al. suggest that olfactory receptors instead developed far later, around the time when vascular plants spread and insects developed the ability to fly.
PMCID: PMC3966513  PMID: 24670956
insect olfactory receptors; Orco; evolution; Lepismachilis y-signata; Thermobia domestica; Phyllium siccifolium; other
11.  The banana code—natural blend processing in the olfactory circuitry of Drosophila melanogaster 
Odor information is predominantly perceived as complex odor blends. For Drosophila melanogaster one of the most attractive blends is emitted by an over-ripe banana. To analyze how the fly's olfactory system processes natural blends we combined the experimental advantages of gas chromatography and functional imaging (GC-I). In this way, natural banana compounds were presented successively to the fly antenna in close to natural occurring concentrations. This technique allowed us to identify the active odor components, use these compounds as stimuli and measure odor-induced Ca2+ signals in input and output neurons of the Drosophila antennal lobe (AL), the first olfactory neuropil. We demonstrate that mixture interactions of a natural blend are very rare and occur only at the AL output level resulting in a surprisingly linear blend representation. However, the information regarding single components is strongly modulated by the olfactory circuitry within the AL leading to a higher similarity between the representation of individual components and the banana blend. This observed modulation might tune the olfactory system in a way to distinctively categorize odor components and improve the detection of suitable food sources. Functional GC-I thus enables analysis of virtually any unknown natural odorant blend and its components in their relative occurring concentrations and allows characterization of neuronal responses of complete neural assemblies. This technique can be seen as a valuable complementary method to classical GC/electrophysiology techniques, and will be a highly useful tool in future investigations of insect-insect and insect-plant chemical interactions.
PMCID: PMC3929855  PMID: 24600405
Drosophila; gas chromatography; in vivo calcium imaging; olfaction; blend coding; insect antennal lobe
12.  Temporal Features of Spike Trains in the Moth Antennal Lobe Revealed by a Comparative Time-Frequency Analysis 
PLoS ONE  2014;9(1):e84037.
The discrimination of complex sensory stimuli in a noisy environment is an immense computational task. Sensory systems often encode stimulus features in a spatiotemporal fashion through the complex firing patterns of individual neurons. To identify these temporal features, we have developed an analysis that allows the comparison of statistically significant features of spike trains localized over multiple scales of time-frequency resolution. Our approach provides an original way to utilize the discrete wavelet transform to process instantaneous rate functions derived from spike trains, and select relevant wavelet coefficients through statistical analysis. Our method uncovered localized features within olfactory projection neuron (PN) responses in the moth antennal lobe coding for the presence of an odor mixture and the concentration of single component odorants, but not for compound identities. We found that odor mixtures evoked earlier responses in biphasic response type PNs compared to single components, which led to differences in the instantaneous firing rate functions with their signal power spread across multiple frequency bands (ranging from 0 to 45.71 Hz) during a time window immediately preceding behavioral response latencies observed in insects. Odor concentrations were coded in excited response type PNs both in low frequency band differences (2.86 to 5.71 Hz) during the stimulus and in the odor trace after stimulus offset in low (0 to 2.86 Hz) and high (22.86 to 45.71 Hz) frequency bands. These high frequency differences in both types of PNs could have particular relevance for recruiting cellular activity in higher brain centers such as mushroom body Kenyon cells. In contrast, neurons in the specialized pheromone-responsive area of the moth antennal lobe exhibited few stimulus-dependent differences in temporal response features. These results provide interesting insights on early insect olfactory processing and introduce a novel comparative approach for spike train analysis applicable to a variety of neuronal data sets.
PMCID: PMC3896344  PMID: 24465391
13.  Dimerisation of the Drosophila odorant coreceptor Orco 
Odorant receptors (ORs) detect volatile molecules and transform this external information into an intracellular signal. Insect ORs are heteromers composed of two seven transmembrane proteins, an odor-specific OrX and a coreceptor (Orco) protein. These ORs form ligand gated cation channels that conduct also calcium. The sensitivity of the ORs is regulated by intracellular signaling cascades. Heterologously expressed Orco proteins form also non-selective cation channels that cannot be activated by odors but by synthetic agonists such as VUAA1. The stoichiometry of OR or Orco channels is unknown. In this study we engineered the simplest oligomeric construct, the Orco dimer (Orco di) and investigated its functional properties. Two Orco proteins were coupled via a 1-transmembrane protein to grant for proper orientation of both parts. The Orco di construct and Orco wild type (Orco wt) proteins were stably expressed in CHO (Chinese Hamster Ovary) cells. Their functional properties were investigated and compared by performing calcium imaging and patch clamp experiments. With calcium imaging experiments using allosteric agonist VUAA1 we demonstrate that the Orco di construct—similar to Orco wt—forms functional calcium conducting ion channel. This was supported by patch clamp experiments. The function of Orco di was seen to be modulated by CaM in a similar manner as the function of Orco wt. In addition, Orco di interacts with the OrX protein, Or22a. The properties of this complex are comparable to Or22a/Orco wt couples. Taken together, the properties of the Orco di construct are similar to those of channels formed by Orco wt proteins. Our results are thus compatible with the view that Orco wt channels are dimeric assemblies.
PMCID: PMC4147393  PMID: 25221476
odorant receptor; coreceptor; concatameric dimer; calmodulin; Orco channel
14.  Expression of ionotropic receptors in terrestrial hermit crab's olfactory sensory neurons 
Coenobitidae are one out of at least five crustacean lineages which independently succeeded in the transition from water to land. This change in lifestyle required adaptation of the peripheral olfactory organs, the antennules, in order to sense chemical cues in the new terrestrial habitat. Hermit crab olfactory aesthetascs are arranged in a field on the distal segment of the antennular flagellum. Aesthetascs house approximately 300 dendrites with their cell bodies arranged in spindle-like complexes of ca. 150 cell bodies each. While the aesthetascs of aquatic crustaceans have been shown to be the place of odor uptake and previous studies identified ionotropic receptors (IRs) as the putative chemosensory receptors expressed in decapod antennules, the expression of IRs besides the IR co-receptors IR25a and IR93a in olfactory sensory neurons (OSNs) has not been documented yet. Our goal was to reveal the expression and distribution pattern of non-co-receptor IRs in OSNs of Coenobita clypeatus, a terrestrial hermit crab, with RNA in situ hybridization. We expanded our previously published RNAseq dataset, and revealed 22 novel IR candidates in the Coenobita antennules. We then used RNA probes directed against three different IRs to visualize their expression within the OSN cell body complexes. Furthermore we aimed to characterize ligand spectra of single aesthetascs by recording local field potentials and responses from individual dendrites. This also allowed comparison to functional data from insect OSNs expressing antennal IRs. We show that this orphan receptor subgroup with presumably non-olfactory function in insects is likely the basis of olfaction in terrestrial hermit crabs.
PMCID: PMC4313712  PMID: 25698921
crustacea; antennules; olfaction; ionotropic receptors; in situ hybridization; electrophysiology
15.  Sense of achievement 
eLife  2013;2:e01605.
Computational techniques developed to predict if odorants will interact with receptors in the olfactory system have achieved a success rate of 70%.
PMCID: PMC3796312  PMID: 24137552
Odorant receptors; antenna; electrophysiology; cheminformatics; D. melanogaster
16.  Host Plant Odors Represent Immiscible Information Entities - Blend Composition and Concentration Matter in Hawkmoths 
PLoS ONE  2013;8(10):e77135.
Host plant choice is of vital importance for egg laying herbivorous insects that do not exhibit brood care. Several aspects, including palatability, nutritional quality and predation risk, have been found to modulate host preference. Olfactory cues are thought to enable host location. However, experimental data on odor features that allow choosing among alternative hosts while still in flight are not available. It has previously been shown that M. sexta females prefer Datura wrightii compared to Nicotiana attenuata. The bouquet of the latter is more intense and contains compounds typically emitted by plants after feeding-damage to attract the herbivore’s enemies. In this wind tunnel study, we offered female gravid hawkmoths (Manduca sexta) odors from these two ecologically relevant, attractive, non-flowering host species. M. sexta females preferred surrogate leaves scented with vegetative odors form both host species to unscented control leaves. Given a choice between species, females preferred the odor bouquet emitted by D. wrightii to that of N. attenuata. Harmonizing, i.e. adjusting, volatile intensity to similar levels did not abolish but significantly weakened this preference. Superimposing, i.e. mixing, the highly attractive headspaces of both species, however, abolished discrimination between scented and non-scented surrogate leaves. Beyond ascertaining the role of blend composition in host plant choice, our results raise the following hypotheses. (i) The odor of a host species is perceived as a discrete odor ‘Gestalt’, and its core properties are lost upon mixing two attractive scents (ii). Stimulus intensity is a secondary feature affecting olfactory-based host choice (iii). Constitutively smelling like a plant that is attracting herbivore enemies may be part of a plant’s strategy to avoid herbivory where alternative hosts are available to the herbivore.
PMCID: PMC3792911  PMID: 24116211
17.  The CCHamide 1 receptor modulates sensory perception and olfactory behavior in starved Drosophila 
Scientific Reports  2013;3:2765.
The olfactory response of the vinegar fly Drosophila melanogaster to food odor is modulated by starvation. Here we show that this modulation is not restricted to food odors and their detecting sensory neurons but rather increases the behavioral response to odors as different as food odors, repellents and pheromones. The increased behavioral responsiveness is paralleled by an increased physiological sensitivity of sensory neurons regardless whether they express olfactory or ionotropic receptors and regardless whether they are housed in basiconic, coeloconic, or trichoid sensilla. Silencing several genes that become up-regulated under starvation confirmed the involvement of the short neuropeptide f receptor in the starvation effect. In addition it revealed that the CCHamide-1 receptor is another important factor governing starvation-induced olfactory modifications.
PMCID: PMC3783891  PMID: 24067446
18.  Intraspecific Combinations of Flower and Leaf Volatiles Act Together in Attracting Hawkmoth Pollinators 
PLoS ONE  2013;8(9):e72805.
Insects pinpoint mates, food and oviposition sites by olfactory cues. Recognizing and localizing a suitable target by olfaction is demanding. Odor sources emit characteristic blends of compounds that have to be identified against an environmentally derived olfactory background. This background, however, does not necessarily disturb the localization of a source. Rather, the contrary. Sex pheromones become more attractive to male moths when being presented against a relevant plant background. Here we asked whether such olfactory coaction also characterizes foraging cues. The tobacco hornworm Manduca sexta feeds on nectar from wild tobacco Nicotiana attenuata and sacred datura Datura wrightii flowers. We tested how leaf-derived volatile blends as a background affect the moths' approach to flower blends. We found coaction when a flower blend was presented against a conspecific leaf volatile background but not when the blend was presented against volatiles emitted by the other host plant or by a non-host plant. Hence, our results reveal a species-specific coaction between flower blend and leaf volatile background. The ability to integrate information from different odor sources on one plant might provide the moth with a fine-grained analysis of food site quality.
PMCID: PMC3771915  PMID: 24069159
19.  Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics 
Arensburger, Peter | Megy, Karine | Waterhouse, Robert M. | Abrudan, Jenica | Amedeo, Paolo | Antelo, Beatriz | Bartholomay, Lyric | Bidwell, Shelby | Caler, Elisabet | Camara, Francisco | Campbell, Corey L. | Campbell, Kathryn S. | Casola, Claudio | Castro, Marta T. | Chandramouliswaran, Ishwar | Chapman, Sinéad B. | Christley, Scott | Costas, Javier | Eisenstadt, Eric | Feshotte, Cedric | Fraser-Liggett, Claire | Guigo, Roderic | Haas, Brian | Hammond, Martin | Hansson, Bill S. | Hemingway, Janet | Hill, Sharon | Howarth, Clint | Ignell, Rickard | Kennedy, Ryan C. | Kodira, Chinnappa D. | Lobo, Neil F. | Mao, Chunhong | Mayhew, George | Michel, Kristin | Mori, Akio | Liu, Nannan | Naveira, Horacio | Nene, Vishvanath | Nguyen, Nam | Pearson, Matthew D. | Pritham, Ellen J. | Puiu, Daniela | Qi, Yumin | Ranson, Hilary | Ribeiro, Jose M. C. | Roberston, Hugh M. | Severson, David W. | Shumway, Martin | Stanke, Mario | Strausberg, Robert | Sun, Cheng | Sutton, Granger | Tu, Zhijian (Jake) | Tubio, Jose Manuel C. | Unger, Maria F. | Vanlandingham, Dana L. | Vilella, Albert J. | White, Owen | White, Jared R. | Wondji, Charles S. | Wortman, Jennifer | Zdobnov, Evgeny M. | Birren, Bruce | Christensen, Bruce M. | Collins, Frank H. | Cornel, Anthony | Dimopoulos, George | Hannick, Linda I. | Higgs, Stephen | Lanzaro, Gregory C. | Lawson, Daniel | Lee, Norman H. | Muskavitch, Marc A. T. | Raikhel, Alexander S. | Atkinson, Peter W.
Science (New York, N.Y.)  2010;330(6000):86-88.
Culex quinquefasciatus (the Southern house mosquito) is an important mosquito vector of viruses such as West Nile virus and St. Louis encephalitis virus as well of nematodes that cause lymphatic filariasis. It is one species within the Culex pipiens species complex and enjoys a distribution throughout tropical and temperate climates of the world. The ability of C. quinquefasciatus to take blood meals from birds, livestock and humans contributes to its ability to vector pathogens between species. We describe the genomic sequence of C. quinquefasciatus, its repertoire of 18,883 protein-coding genes is 22% larger than Ae. aegypti and 52% larger than An. gambiae with multiple gene family expansions including olfactory and gustatory receptors, salivary gland genes, and genes associated with xenobiotic detoxification.
PMCID: PMC3740384  PMID: 20929810
20.  Divergence in Olfactory Host Plant Preference in D. mojavensis in Response to Cactus Host Use 
PLoS ONE  2013;8(7):e70027.
Divergence in host adaptive traits has been well studied from an ecological and evolutionary perspective, but identification of the proximate mechanisms underlying such divergence is less well understood. Behavioral preferences for host plants are often mediated by olfaction and shifts in preference may be accompanied by changes in the olfactory system. In this study, we examine the evolution of host plant preferences in cactophilic Drosophila mojavensis that feeds and breeds on different cacti throughout its range. We show divergence in electrophysiological responses and olfactory behavior among populations with host plant shifts. Specifically, significant divergence was observed in the Mojave Desert population that specializes on barrel cactus. Differences were observed in electrophysiological responses of the olfactory organs and in behavioral responses to barrel cactus volatiles. Together our results suggest that the peripheral nervous system has changed in response to different ecological environments and that these changes likely contribute to divergence among D. mojavensis populations.
PMCID: PMC3723661  PMID: 23936137
21.  Flexible weighing of olfactory and vector information in the desert ant Cataglyphis fortis 
Biology Letters  2013;9(3):20130070.
Desert ants, Cataglyphis fortis, are equipped with remarkable skills that enable them to navigate efficiently. When travelling between the nest and a previously visited feeding site, they perform path integration (PI), but pinpoint the nest or feeder by following odour plumes. Homing ants respond to nest plumes only when the path integrator indicates that they are near home. This is crucial, as homing ants often pass through plumes emanating from foreign nests and do not discriminate between the plume of their own and that of a foreign nest, but should absolutely avoid entering a wrong nest. Their behaviour towards food odours differs greatly. Here, we show that in ants on the way to food, olfactory information outweighs PI information. Although PI guides ants back to a learned feeder, the ants respond to food odours independently of whether or not they are close to the learned feeding site. This ability is beneficial, as new food sources—unlike foreign nests—never pose a threat but enable ants to shorten distances travelled while foraging. While it has been shown that navigating C. fortis ants rely strongly on PI, we report here that the ants retained the necessary flexibility in the use of PI.
PMCID: PMC3645040  PMID: 23594568
Cataglyphis; path integration; odour plume; homing; foraging; navigation
22.  Correction: Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition 
eLife  2013;2:e00992.
PMCID: PMC3679526
Manduca sexta; plant volatiles; oviposition; Ca imaging; Datura wrightii; Other
23.  Host plant-driven sensory specialization in Drosophila erecta 
Finding appropriate feeding and breeding sites is crucial for all insects. To fulfil this vital task, many insects rely on their sense of smell. Alterations in the habitat—or in lifestyle—should accordingly also be reflected in the olfactory system. Solid functional evidence for direct adaptations in the olfactory system is however scarce. We have, therefore, examined the sense of smell of Drosophila erecta, a close relative of Drosophila melanogaster and specialist on screw pine fruits (Pandanus spp.). In comparison with three sympatric sibling species, D. erecta shows specific alterations in its olfactory system towards detection and processing of a characteristic Pandanus volatile (3-methyl-2-butenyl acetate, 3M2BA). We show that D. erecta is more sensitive towards this substance, and that the increased sensitivity derives from a numerical increase of one olfactory sensory neuron (OSN) class. We also show that axons from these OSNs form a complex of enlarged glomeruli in the antennal lobe, the first olfactory brain centre, of D. erecta. Finally, we show that 3M2BA induces oviposition in D. erecta, but not in D. melanogaster. The presumed adaptations observed here follow to a remarkable degree those found in Drosophila sechellia, a specialist upon noni fruit, and suggest a general principle for how specialization affects the sense of smell.
PMCID: PMC3652467  PMID: 23595274
insect olfaction; specialization; Drosophila; oviposition
24.  Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition 
eLife  2013;2:e00421.
The ability to decrypt volatile plant signals is essential if herbivorous insects are to optimize their choice of host plants for their offspring. Green leaf volatiles (GLVs) constitute a widespread group of defensive plant volatiles that convey a herbivory-specific message via their isomeric composition: feeding of the tobacco hornworm Manduca sexta converts (Z)-3- to (E)-2-GLVs thereby attracting predatory insects. Here we show that this isomer-coded message is monitored by ovipositing M. sexta females. We detected the isomeric shift in the host plant Datura wrightii and performed functional imaging in the primary olfactory center of M. sexta females with GLV structural isomers. We identified two isomer-specific regions responding to either (Z)-3- or (E)-2-hexenyl acetate. Field experiments demonstrated that ovipositing Manduca moths preferred (Z)-3-perfumed D. wrightii over (E)-2-perfumed plants. These results show that (E)-2-GLVs and/or specific (Z)-3/(E)-2-ratios provide information regarding host plant attack by conspecifics that ovipositing hawkmoths use for host plant selection.
eLife digest
Plants have developed a variety of strategies to defend themselves against herbivorous animals, particularly insects. In addition to mechanical defences such as thorns and spines, plants also produce compounds known as secondary metabolites that keep insects and other herbivores at bay by acting as repellents or toxins. Some of these metabolites are produced on a continuous basis by plants, whereas others—notably compounds called green-leaf volatiles—are only produced once the plant has been attacked. Green-leaf volatiles—which are also responsible for the smell of freshly cut grass—have been observed to provide plants with both direct protection, by inhibiting or repelling herbivores, and indirect protection, by attracting predators of the herbivores themselves.
The hawkmoth Manduca sexta lays its eggs on various plants, including tobacco plants and sacred Datura plants. Once the eggs have hatched into caterpillars, they start eating the leaves of their host plant, and if present in large numbers, these caterpillars can quickly defoliate and destroy it. In an effort to defend itself, the host plant releases green-leaf volatiles to attract various species of Geocoris, and these bugs eat the eggs.
One of the green-leaf volatiles released by tobacco plants is known as (Z)-3-hexenal, but enzymes released by M. sexta caterpillars change some of these molecules into (E)-2-hexenal, which has the same chemical formula but a different structure. The resulting changes in the ‘volatile profile’ alerts Geocoris bugs to the presence of M. sexta eggs and caterpillars on the plant.
Now Allmann et al. show that adult female M. sexta moths can also detect similar changes in the volatile profile emitted by sacred Datura plants that have been damaged by M. sexta caterpillars. This alerts the moths to the fact that Geocoris bugs are likely to be attacking eggs and caterpillars on the plant, or on their way to the plant, so they lay their eggs on other plants. This reduces competition for resources and also reduces the risk of newly laid eggs being eaten by predators. Allmann et al. also identified the neural mechanism that allows moths to detect changes in the volatile profile of plants—the E- and Z- odours lead to different activation patterns in the moth brain.
PMCID: PMC3654435  PMID: 23682312
Manduca sexta; plant volatiles; oviposition; Ca imaging; Datura wrightii; Other
25.  In situ Tip-Recordings Found No Evidence for an Orco-Based Ionotropic Mechanism of Pheromone-Transduction in Manduca sexta 
PLoS ONE  2013;8(5):e62648.
The mechanisms of insect odor transduction are still controversial. Insect odorant receptors (ORs) are 7TM receptors with inverted membrane topology. They colocalize with a conserved coreceptor (Orco) with chaperone and ion channel function. Some studies suggest that insects employ exclusively ionotropic odor transduction via OR-Orco heteromers. Other studies provide evidence for different metabotropic odor transduction cascades, which employ second messenger-gated ion channel families for odor transduction. The hawkmoth Manduca sexta is an established model organism for studies of insect olfaction, also due to the availability of the hawkmoth-specific pheromone blend with its main component bombykal. Previous patch-clamp studies on primary cell cultures of M. sexta olfactory receptor neurons provided evidence for a pheromone-dependent activation of a phospholipase Cβ. Pheromone application elicited a sequence of one rapid, apparently IP3-dependent, transient and two slower Ca2+-dependent inward currents. It remains unknown whether additionally an ionotropic pheromone-transduction mechanism is employed. If indeed an OR-Orco ion channel complex underlies an ionotropic mechanism, then Orco agonist-dependent opening of the OR-Orco channel pore should add up to pheromone-dependent opening of the pore. Here, in tip-recordings from intact pheromone-sensitive sensilla, perfusion with the Orco agonist VUAA1 did not increase pheromone-responses within the first 1000 ms. However, VUAA1 increased spontaneous activity of olfactory receptor neurons Zeitgebertime- and dose-dependently. We conclude that we find no evidence for an Orco-dependent ionotropic pheromone transduction cascade in M. sexta. Instead, in M. sexta Orco appears to be a slower, second messenger-dependent pacemaker channel which affects kinetics and threshold of pheromone-detection via changes of intracellular Ca2+ baseline concentrations.
PMCID: PMC3643954  PMID: 23671617

Results 1-25 (64)