Schreckstoff: It takes two to panic.

Schreckstoff (fear substance) is an alarm signal released by injured fish that induces a fear response. Its chemical nature has long been debated. A new study finds that zebrafish Schreckstoff is composed of at least three components, two of which elicit the fear response only in combination.

Insect genomics: A lousy fly.

The bee louse (Braula coeca) is a honeybee inquiline and a long-standing taxonomic mystery. A new study unravels their genomic architecture and shows that these enigmatic flies have evolved from scale insect-exploiting drosophilid ancestors and share genetic similarities with their honeybee hosts.

Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution.

The ability to perform genomic sequencing on long-dead organisms is opening new frontiers in evolutionary research. These opportunities are especially notable in the case of museum collections, from which countless documented specimens may now be suitable for genomic analysis-if data of sufficient quality can be obtained. Here, we report 25 newly sequenced genomes from museum specimens of the model organism Drosophila melanogaster, including the oldest extant specimens of this species. By comparing historical samples ranging from the early 1800s to 1933 against modern-day genomes, we document evolution across thousands of generations, including time periods that encompass the species' initial occupation of northern Europe and an era of rapidly increasing human activity. We also find that the Lund, Sweden population underwent local genetic differentiation during the early 1800s to 1933 interval (potentially due to drift in a small population) but then became more similar to other European populations thereafter (potentially due to increased migration). Within each century-scale time period, our temporal sampling allows us to document compelling candidates for recent natural selection. In some cases, we gain insights regarding previously implicated selection candidates, such as ChKov1, for which our inferred timing of selection favors the hypothesis of antiviral resistance over insecticide resistance. Other candidates are novel, such as the circadian-related gene Ahcy, which yields a selection signal that rivals that of the DDT resistance gene Cyp6g1. These insights deepen our understanding of recent evolution in a model system, and highlight the potential of future museomic studies.

Neuroscience: Flies and grits.

Food texture affects palatability. A new study finds that the common dew fly Drosophila melanogaster is also choosy when it comes to food texture. Flies evaluate size and presence of food particles through neurons in the tongue that express the mechanically activated channel protein TMEM63.

The irritant receptor TRPA1 mediates the mosquito repellent effect of catnip.

Catnip (Nepeta cataria) is a common garden herb well known for its euphoric and hallucinogenic effects on domestic cats,1-3 for its medicinal properties,4,5 as well as for its powerful repellent action on insects.6,7 Catnip extracts have been proposed as a natural alternative to synthetic insect repellents, such as N,N-diethyl-3-methylbenzamide (DEET),8,9 but how catnip triggers aversion in insects is not known. Here, we show that, both in Drosophila melanogaster flies and Aedes aegypti mosquitoes, the major mediator of catnip repellency is the widely conserved chemical irritant receptor TRPA1. In vitro, both catnip extract and its active ingredient nepetalactone can directly activate fly and mosquito TRPA1. In vivo, D. melanogaster and Ae. aegypti TRPA1 mutants are no longer repelled by catnip and nepetalactone. Interestingly, our data show that some, but not all, fly and mosquito TRPA1 variants are catnip targets. Moreover, unlike the broad TRPA1 agonist allyl isothiocyanate (AITC) (an active ingredient of tear gas and wasabi), catnip does not activate human TRPA1. Our results support the use of catnip and nepetalactone as insect-selective irritants and suggest that, despite TRPA1's broad conservation, insect TRPA1 can be targeted for the development of safe repellents.

Neuroscience: The Secret of Sauce Béarnaise Syndrome Is in the Circuit.

During conditioned food aversion - a.k.a. sauce béarnaise syndrome - the ingestion of a spoiled food item leads to a lasting aversion towards cues reminiscent of the item. A new study finds that, in Drosophila, taste aversion depends on the immune system and the mushroom body.

Mosquito Biology: How a Quest for Water Spawned a Thirst for Blood.

The invasive yellow-fever mosquito Aedes aegypti preferentially feeds on human blood. A new study finds that human-biting in this important disease vector might just be an unfortunate side effect of breeding in human-stored water.

Geosmin Attracts Aedes aegypti Mosquitoes to Oviposition Sites.

Geosmin is one of the most recognizable and common microbial smells on the planet. Some insects, like mosquitoes, require microbial-rich environments for their progeny, whereas for other insects such microbes may prove dangerous. In the vinegar fly Drosophila melanogaster, geosmin is decoded in a remarkably precise fashion and induces aversion, presumably signaling the presence of harmful microbes [1]. We have here investigated the effect of geosmin on the behavior of the yellow fever mosquito Aedes aegypti. In contrast to flies, geosmin is not aversive but mediates egg-laying site selection. Female mosquitoes likely associate geosmin with microbes, including cyanobacteria consumed by larvae [2], who also find geosmin-as well as geosmin-producing cyanobacteria-attractive. Using in vivo multiphoton calcium imaging from transgenic PUb-GCaMP6s mosquitoes, we show that Ae. aegypti code geosmin in a qualitatively similar fashion to flies, i.e., through a single olfactory channel with a high degree of sensitivity for this volatile. We further demonstrate that geosmin can be used as bait under field conditions, and finally, we show that geosmin, which is both expensive and difficult to obtain, can be substituted by beetroot peel extract, providing a cheap and viable potential mean for mosquito control and surveillance in developing countries.

Recurrent Collection of Drosophila melanogaster from Wild African Environments and Genomic Insights into Species History.

A long-standing enigma concerns the geographic and ecological origins of the intensively studied vinegar fly, Drosophila melanogaster. This globally distributed human commensal is thought to originate from sub-Saharan Africa, yet until recently, it had never been reported from undisturbed wilderness environments that could reflect its precommensal niche. Here, we document the collection of 288 D. melanogaster individuals from multiple African wilderness areas in Zambia, Zimbabwe, and Namibia. The presence of D. melanogaster in these remote woodland environments is consistent with an ancestral range in southern-central Africa, as opposed to equatorial regions. After sequencing the genomes of 17 wilderness-collected flies collected from Kafue National Park in Zambia, we found reduced genetic diversity relative to town populations, elevated chromosomal inversion frequencies, and strong differences at specific genes including known insecticide targets. Combining these genomes with existing data, we probed the history of this species' geographic expansion. Demographic estimates indicated that expansion from southern-central Africa began ∼10,000 years ago, with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,400 years ago. This improved model of demographic history will provide an important resource for future evolutionary and genomic studies of this key model organism. Our findings add context to the history of D. melanogaster, while opening the door for future studies on the biological basis of adaptation to human environments.

Aedes aegypti Mosquitoes Detect Acidic Volatiles Found in Human Odor Using the IR8a Pathway.

Mosquitoes use olfaction as a primary means of detecting their hosts. Previously, the functional ablation of a family of Aedes aegypti olfactory receptors, the odorant receptors (ORs), was not sufficient to reduce host seeking in the presence of carbon dioxide (CO2). This suggests the olfactory receptors that remain, such as the ionotropic receptors (IRs), could play a significant role in host detection. To test this, we disrupted the Ir8a co-receptor in Ae. aegypti using CRISPR/Cas9. We found that Ir8a mutant female mosquitoes are not attracted to lactic acid, a behaviorally active component of human sweat, and they lack odor-evoked responses to acidic volatiles. The loss of Ir8a reduces mosquito attraction to humans and their odor. We show that the CO2-detection pathway is necessary but not sufficient for IR8a to detect human odor. Our study reveals that the IR8a pathway is crucial for an anthropophilic vector mosquito to effectively seek hosts. VIDEO ABSTRACT.

Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit.

Although the vinegar fly Drosophila melanogaster is arguably the most studied organism on the planet, fundamental aspects of this species' natural ecology have remained enigmatic [1]. We have here investigated a wild population of D. melanogaster from a mopane forest in Zimbabwe. We find that these flies are closely associated with marula fruit (Sclerocarya birrea) and propose that this seasonally abundant and predominantly Southern African fruit is a key ancestral host of D. melanogaster. Moreover, when fruiting, marula is nearly exclusively used by D. melanogaster, suggesting that these forest-dwelling D. melanogaster are seasonal specialists, in a similar manner to, e.g., Drosophila erecta on screw pine cones [2]. We further demonstrate that the main chemicals released by marula activate odorant receptors that mediate species-specific host choice (Or22a) [3, 4] and oviposition site selection (Or19a) [5]. The Or22a-expressing neurons-ab3A-respond strongly to the marula ester ethyl isovalerate, a volatile rarely encountered in high amounts in other fruit. We also show that Or22a differs among African populations sampled from a wide range of habitats, in line with a function associated with host fruit usage. Flies from Southern Africa, most of which carry a distinct allele at the Or22a/Or22b locus, have ab3A neurons that are more sensitive to ethyl isovalerate than, e.g., European flies. Finally, we discuss the possibility that marula, which is also a culturally and nutritionally important resource to humans, may have helped the transition to commensalism in D. melanogaster.

Insect Olfaction: Once Swatted, Twice Shy.

While some mosquitoes are known to have an innate penchant for human hosts, new research details that they can learn, what they can learn and how they can learn.

Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain.

The Drosophila antenna contains receptor neurons for mechanical, olfactory, thermal, and humidity stimuli. Neurons expressing the ionotropic receptor IR40a have been implicated in the selection of an appropriate humidity range [1, 2], but although previous work indicates that insect hygroreceptors may be made up by a "triad" of neurons (with a dry-, a cold-, and a humid-air-responding cell [3]), IR40a expression included only cold- and dry-air cells. Here, we report the identification of the humid-responding neuron that completes the hygrosensory triad in the Drosophila antenna. This cell type expresses the Ir68a gene, and Ir68a mutation perturbs humidity preference. Next, we follow the projections of Ir68a neurons to the brain and show that they form a distinct glomerulus in the posterior antennal lobe (PAL). In the PAL, a simple sensory map represents related features of the external environment with adjacent "hot," "cold," "dry," and "humid" glomeruli-an organization that allows for both unique and combinatorial sampling by central relay neurons. Indeed, flies avoided dry heat more robustly than humid heat, and this modulation was abolished by silencing of dry-air receptors. Consistently, at least one projection neuron type received direct synaptic input from both temperature and dry-air glomeruli. Our results further our understanding of humidity sensing in the Drosophila antenna, uncover a neuronal substrate for early sensory integration of temperature and humidity in the brain, and illustrate the logic of how ethologically relevant combinations of sensory cues can be processed together to produce adaptive behavioral responses.

Sensory Evolution: Trouble in the Cherry Orchard.

Understanding how and why some species become pests, while their relatives remain harmless, might help us control them. A new study looks at how sensory mechanisms evolved in an emerging pest fly species.

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance.

BACKGROUND: The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. RESULTS: We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. CONCLUSIONS: The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

Evolutionary Genetics: Smells like a Pseudo-pseudogene.

A new study reports the presence of a chemosensory pseudogene in Drosophila sechellia, which in spite of carrying a premature stop-codon nevertheless encodes a fully functional and full-length protein. Such 'pseudo-pseudogenes' might well be a widespread phenomenon.

Fecal-Derived Phenol Induces Egg-Laying Aversion in Drosophila.

Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by members of the order Diptera, i.e., flies. How Drosophila melanogaster reacts to fecal matter remains unclear. Here, we examined oviposition behavior toward a range of fecal samples from mammals native to the putative Southeast African homeland of the fly. We show that D. melanogaster display a strong oviposition aversion toward feces from carnivorous mammals but indifference or even attraction toward herbivore dung. We identify a set of four predictor volatiles, which can be used to differentiate fecal from non-fecal matter, as well as separate carnivore from herbivore feces. Of these volatiles, phenol-indicative of carnivore feces-confers egg-laying aversion and is detected by a single class of sensory neurons expressing Or46a. The Or46a-expressing neurons are necessary and sufficient for oviposition site aversion. We further demonstrate that carnivore feces-unlike herbivore dung-contain a high rate of pathogenic bacteria taxa. These harmful bacteria produce phenol from L-tyrosine, an amino acid specifically enriched in high protein diets, such as consumed by carnivores. Finally, we demonstrate that carnivore feces, as well as phenol, is also avoided by a ball-rolling species of dung beetle, suggesting that phenol is a widespread avoidance signal because of its association with pathogenic bacteria.

Humidity Sensing in Drosophila.

Environmental humidity influences the fitness and geographic distribution of all animals [1]. Insects in particular use humidity cues to navigate the environment, and previous work suggests the existence of specific sensory mechanisms to detect favorable humidity ranges [2-5]. Yet, the molecular and cellular basis of humidity sensing (hygrosensation) remains poorly understood. Here we describe genes and neurons necessary for hygrosensation in the vinegar fly Drosophila melanogaster. We find that members of the Drosophila genus display species-specific humidity preferences related to conditions in their native habitats. Using a simple behavioral assay, we find that the ionotropic receptors IR40a, IR93a, and IR25a are all required for humidity preference in D. melanogaster. Yet, whereas IR40a is selectively required for hygrosensory responses, IR93a and IR25a mediate both humidity and temperature preference. Consistent with this, the expression of IR93a and IR25a includes thermosensory neurons of the arista. In contrast, IR40a is excluded from the arista but is expressed (and required) in specialized neurons innervating pore-less sensilla of the sacculus, a unique invagination of the third antennal segment. Indeed, calcium imaging showed that IR40a neurons directly respond to changes in humidity, and IR40a knockdown or IR93a mutation reduced their responses to stimuli. Taken together, our results suggest that the preference for a specific humidity range depends on specialized sacculus neurons, and that the processing of environmental humidity can happen largely in parallel to that of temperature.

Drosophila Avoids Parasitoids by Sensing Their Semiochemicals via a Dedicated Olfactory Circuit.

Detecting danger is one of the foremost tasks for a neural system. Larval parasitoids constitute clear danger to Drosophila, as up to 80% of fly larvae become parasitized in nature. We show that Drosophila melanogaster larvae and adults avoid sites smelling of the main parasitoid enemies, Leptopilina wasps. This avoidance is mediated via a highly specific olfactory sensory neuron (OSN) type. While the larval OSN expresses the olfactory receptor Or49a and is tuned to the Leptopilina odor iridomyrmecin, the adult expresses both Or49a and Or85f and in addition detects the wasp odors actinidine and nepetalactol. The information is transferred via projection neurons to a specific part of the lateral horn known to be involved in mediating avoidance. Drosophila has thus developed a dedicated circuit to detect a life-threatening enemy based on the smell of its semiochemicals. Such an enemy-detecting olfactory circuit has earlier only been characterized in mice and nematodes.