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Hansson, B. S.

Publications and source records attributed to Hansson, B. S..

34 records · Page 2Linked to original sources

Comparative dissection of the peripheral olfactory system of the Chagas disease vectors Rhodnius prolixus and Rhodnius brethesi

American trypanosomiasis or Chagas disease is thought to be transmitted by both domestic and sylvatic species of Triatominae. These haematophagous insects use sensory cues to find their vertebrate hosts. Among them, odorants have been shown to play a key role. Previous work revealed morphological differences in the sensory apparatus of sylvatic and domestic species of Triatomines, but to date a functional study of the olfactory system is not available. After examining the antennal sensilla with scanning electronic microscopy (SEM), we compared olfactory responses of the domestic Rhodnius prolixus and the sylvatic Rhodnius brethesi with an electrophysiological approach. In electroantennogram (EAG) recordings, we first show that the antenna of R. prolixus shows high responses to carboxylic acids, compounds found in their habitat and headspace of hosts. We then compared responses from olfactory sensory neurons (OSNs) housed in the grooved peg sensilla of both species as these are tuned to these compounds using single-sensillum recordings (SSR). In R. prolixus, the SSR responses revealed a narrower tuning breath than its sylvatic counterpart, with the latter showing responses to a broader range of chemical classes. Additionally, we observed significant differences between these two species in their response to particular volatiles, such as amyl acetate and butyryl chloride. In summary, the closely related, but ecologically differentiated R. prolixus and R. brethesi display distinct differences in their olfactory functions. Considering the ongoing rapid destruction of the natural habitat of sylvatic species and likely shifts towards environments shaped by humans, we expect that our results will contribute to the design of efficient vector control strategies in the future. Author SummaryAmerican Tripanosomiasis, also known as Chagas disease, is a disease which no one speaks out, although there are up to eight million people infected worldwide. Its causative agent is the protozoan Tripanosoma cruzi which is transmitted by triatomine insects, alias kissing bugs. Several studies have highlighted the importance of olfaction for host-seeking behavior in these insects, which enables them to target their vertebrate hosts, and to get their vital blood meal, while infecting them at the same time. Vector control strategies have been the most efficient policy to combat the spread of Chagas disease by triatomine insects. However, recent changes in the natural habitats of these insects challenge their effectiveness, as species so far thought to be exclusive to sylvatic environments are now frequently found in peridomestic areas. In this context, to understand how sylvatic and domestic kissing bugs detect odors to locate their host and choose their habitats is highly relevant. In this study, we compare the olfactory system of the domestic kissing bug Rhodnius prolixus and its sylvatic counterpart Rhodnius brethesi at a morphological and functional level. We reveal that detection of host and habitat volatiles share many similarities, but also exhibit pronounced differences between both species.

ecology↗

Large-scale characterization of sex pheromone communication systems in Drosophila

Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Despite the profound knowledge of sex pheromones, little is known about the coevolutionary mechanisms and constraints on their production and detection. Using whole-genome sequences to infer the kinship among 99 drosophilids, we investigate how phylogenetic and chemical traits have interacted at a wide evolutionary timescale. Through a series of chemical syntheses and electrophysiological recordings, we identify 51 sex-specific compounds, many of which are detected via olfaction. Behavioral analyses reveal that many of the 42 male-specific compounds are transferred to the female during copulation and mediate female receptivity and/or male courtship inhibition. Measurement of phylogenetic signals demonstrates that sex pheromones and their cognate olfactory channels evolve rapidly and independently over evolutionary time to guarantee efficient intra- and inter-specific communication systems. Our results show how sexual isolation barriers between species can be reinforced by species-specific olfactory signals.

evolutionary biology↗

Alcohol boosts pheromone production in male flies and makes them sexier

The attraction of Drosophila melanogaster towards byproducts of alcoholic fermentation, especially ethanol, has been extensively studied 1-4. However, the adaptive value of this behavior has not been elucidated. Previous studies have suggested anthropomorphic interpretations of D. melanogaster behavior towards alcohols 5,6. Here, we instead assert that there exists a simple yet vital biological rationale for alcohol contact and consumption by these insects. We show that exposure to alcohols, especially methanol, results in an immediate amplification of fatty acid ester pheromone levels, which in turn elevates the probability that a male will successfully compete for a female during courtship. We proceed to identify three types of olfactory sensory neurons that detect ethanol and methanol. Moreover, we trace the ensuing neural circuits and reveal their role in controlling both attraction and aversion, where valence is balanced around mating status. Based on our results, we deduce that male flies associate with sources of alcohol as a biological imperative related to reproduction, and we provide an assessment of how and why D. melanogaster is associated with alcohol using a sound ecological and natural history approach to this previously enigmatic biological phenomenon. One sentence summaryFlies gain pheromone and courtship advantages with alcohol, but methanol is toxic, thus flies must balance risk versus reward.

neuroscience↗

Comparative morphological and transcriptomic analyses reveal novel chemosensory genes in the poultry red mite, Dermanyssus gallinae and knockdown by RNA interference

Detection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators. The current knowledge of how chemical cues are detected is based primarily on data acquired from studies on insects, while our understanding of the molecular basis for chemoreception in acari, mites in particular, remains limited. The poultry red mite (PRM), Dermanyssus gallinae, is one of the most important blood-feeding ectoparasites of poultry. Unlike other ectoparasites on animals, PRM feeds mainly at night. During daytime, these animals hide themselves in crevices around the poultry house. The diversity in habitat usage, as well as the demonstrated host finding and avoidance behaviors suggest that PRM relies on their sense of smell to orchestrate complex behavioral decisions. Comparative transcriptome analyses revealed the presence of candidate variant ionotropic receptors (IRs), odorant binding proteins (OBPs), niemann-pick proteins type C2 (NPC2) and sensory neuron membrane proteins (SNMPs). Some of these proteins were highly and differentially expressed in the forelegs of PRM. Rhodopsin-like G protein-coupled receptors (GPCRs) were also identified, while insect-specific odorant receptors (ORs) and odorant co-receptors (ORcos) were not detected. Furthermore, using scanning electron microscopy (SEM), the tarsomeres of all legs pairs were shown to be equipped with sensilla chaetica with or without tip pores, while wall-pored olfactory sensilla chaetica were restricted to the distal-most tarsomeres of the forelegs. Further, using the conserved odorant binding protein (OBP) as a test case, the results showed that RNA interference (RNAi) can be induced in D. gallinae chemosensory tissues. This study is the first to describe the presence of chemosensory genes in any Dermanyssidae family. It is also the first report of chemosensory gene knockdown by RNAi in any mite species and demonstrate that their diminutive size, less than 1 mm, is not a major impediment when applying gene knockdown approaches. Our findings make a significant step forward in understanding the chemosensory abilities of D. gallinae.

molecular biology↗

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

AO_SCPLOWBSTRACTC_SCPLOWBark beetle behavior is to a large extent mediated via olfaction. Targeting the odorant receptors (ORs) may thus provide avenues towards improved pest control during outbreaks. Such an approach requires information on the function of receptors and their interactions with ligands. Hence, we annotated 73 ORs from an antennal transcriptome of the spruce bark beetle Ips typographus and report the functional characterization of two ORs (ItypOR46 and ItypOR49), which are selective for single enantiomers of the common bark beetle pheromone compounds ipsenol and ipsdienol, respectively. We use homology modeling and molecular docking to predict their binding sites. The importance of residues Tyr84 and Thr205 in ItypOR46 in the activation by ipsenol is experimentally supported, and hydrogen bonding appears key in pheromone binding. The biological significance of the characterized ORs positions them as prime targets for pest control and use in biosensors to detect bark beetle infestations.

neuroscience↗

Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.

neuroscience↗

The olfactory co-receptor IR8a governs larval-frass mediated competition avoidance in a hawkmoth

Finding a suitable oviposition site is a challenging task for a gravid female moth. At the same time, it is of paramount importance considering the limited capability of most caterpillars to relocate to alternative host plants. The hawkmoth, Manduca sexta (Sphingidae), oviposits on solanaceous plants. Larvae hatching on a plant that is already attacked by conspecific caterpillars can face food competition, as well as an increased exposure to predators and induced plant defenses. Here, we show that frass from conspecific caterpillars is sufficient to deter a female M. sexta from ovipositing on a plant and that this deterrence is based on the frass-emitted carboxylic acids 3-methylpentanoic acid and hexanoic acid. Using a combination of genome editing (CRISPR/Cas9), electrophysiological recordings, calcium imaging and behavioral analyses we demonstrate that the ionotropic co-receptor IR8a is essential for acid-mediated frass avoidance in ovipositing hawkmoths.

neuroscience↗

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Comparative analysis of multiple genomes has been used extensively to examine the evolution of chemosensory receptors across the genus Drosophila. However, few studies have delved into functional characteristics, as most have relied exclusively on genomic data alone, especially for non-model species. In order to increase our understanding of olfactory evolution, we have generated a comprehensive assessment of the olfactory functions associated with the antenna and palps for Drosophila suzukii as well as several other members of the subgenus Sophophora, thus creating a functional olfactory landscape across a total of 20 species. Here we identify and describe several common elements of evolution, including consistent changes in ligand spectra as well as relative receptor abundance, which appear heavily correlated with the known phylogeny. We also combine our functional ligand data with protein orthologue alignments to provide a high-throughput evolutionary assessment and predictive model, where we begin to examine the underlying mechanisms of evolutionary changes utilizing both genetics and odorant binding affinities. In addition, we document that only a few receptors frequently vary between species, and we evaluate the justifications for evolution to reoccur repeatedly within only this small subset of available olfactory sensory neurons.

evolutionary biology↗

Niche partitioning as a selective pressure for the evolution of the Drosophila nervous system

The ecological and developmental selective pressures associated with evolution have shaped most animal traits, such as behavior, morphology and neurobiology. As such, the examination of phylogenetic characteristics of the nervous system can be utilized as a means to assess these traits, and thus, to evaluate the underlying selective pressures that produce evolutionary variation between species. Recent studies across a multitude of Drosophila have hypothesized the existence of a fundamental tradeoff between two primary sensory organs, the eye and the antenna. However, the identification of any potential ecological mechanisms for this observed tradeoff have not been firmly established. Our current study examines two monophyletic species within the obscura group, and asserts that despite their close relatedness and overlapping ecology, they deviate strongly in both visual and olfactory investment. Here we contend that both courtship and microhabitat preferences mirror and support the observed inverse variation in these sensory traits. Moreover, that this variation in visual and olfactory investment between closely-related species seems to provide relaxed competition, a process by which similar species can use a shared environment differently and in ways that help them both coexist. The nervous system has a unique role in evolution as it provides the functional connection between morphology, physiology, and behavior. As such, characterizing any tradeoffs between costs and benefits for the nervous system may be essential to our understanding of animal diversity, as well as vital to our understanding of the selective forces that have shaped the natural world.

evolutionary biology↗

Optimization of insect odorant receptor trafficking and functional expression via transient transfection in HEK293 cells

Insect odorant receptors show a limited functional expression in various heterologous expression systems including insect and mammalian cells. This may be in part due to the absence of key components driving the release of these proteins from the endoplasmic reticulum and directing them to the plasma membrane. In order to mitigate this problem we took advantage of small export signals within the human HCN1 and Rhodopsin that have been shown to promote protein release from the endoplasmic reticulum and the trafficking of post-Golgi vesicles, respectively. Moreover, we designed a new vector based on a bidirectional expression cassette to drive the functional expression of the insect odorant receptor co-receptor (Orco) and an odor-binding odorant receptor, simultaneously. We show that this new method can be used to reliably express insect odorant receptors in HEK293 cells via transient transfection and that is highly suitable for downstream applications using automated and high-throughput imaging platforms.

zoology↗

Learning may help pollinators find their host plants in polluted landscapes

Pollination strongly contributes to food production, and often relies on pollinating insects. However, atmospheric pollution may interfere with pollination by disrupting floral plumes that pollinators use to navigate to flowers.\n\nIn this study, we examine the impacts of pollution-induced elevated ozone levels on the composition of a floral blend of Nicotiana alata and examine the response of innate and trained Manduca sexta to the ozone-altered blend.\n\nOzone exposure altered the floral blend of N. alata, and disrupted the innate attraction of naive M. sexta to the altered blend. However, associative learning can offset this disruption in attraction. Moths that were enticed with visual cues to an artificial flower emitting an ozonated blend learned to associate this blend with a nectar reward after just one rewarded experience. More importantly, moths that were rewarded while experiencing the unozonated floral blend of their host subsequently found the ozonated floral blend of the same host attractive, most likely due to experience-based reinforcement of ozone-insensitive cues in the blend.\n\nThe attraction of moths to both unaltered and ozonated plumes is critical for tolerating polluted landscapes. At the host plant, where moths feed, floral emissions are relatively pure. As floral odors travel away from the host, however, they become degraded by pollution. Therefore, targeting the flower requires recognizing both conditions of the odor. The ability to generalize between the pure and ozone-altered scents may enable pollinators like M. sexta to maintain communication with their flowers and reduce the impact anthropogenic oxidants may have on plant-pollinator systems.

animal behavior and cognition↗

Functional integration of \"undead\" neurons in the olfactory system

Programmed cell death (PCD) is widespread during neurodevelopment, typically eliminating the surpluses of neuronal production. Employing the Drosophila olfactory system, we examined the potential of cells fated to die to contribute to circuit evolution. Inhibition of PCD is sufficient to generate many new cells that express neural markers and exhibit odor-evoked activity. These \"undead\" neurons express a subset of olfactory receptors that, intriguingly, is enriched for recent receptor duplicates and include some normally found in other chemosensory organs and life-stages. Moreover, undead neuron axons integrate into the olfactory circuitry in the brain, forming novel receptor/glomerular couplings. Comparison of homologous olfactory lineages across drosophilids reveals natural examples of fate changes from death to a functional neuron. Finally, we provide evidence that PCD contributes to evolutionary differences in carbon dioxide-sensing circuit formation in Drosophila and mosquitoes. These results reveal the remarkable potential of alterations in PCD patterning to evolve new neural pathways.

neuroscience↗

Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

The insect odorant receptor (Or) gene family is among the largest multigene families in insect genomes, but its evolutionary origin and mode of expansion is still a matter of debate. We performed transcriptomic surveys of two wingless insect species, the silverfish Lepisma saccharina and Tricholepidion gertschi, and identified multiple Or gene family members in both species. A phylogenetic analysis suggests that the silverfish Ors do not fall into the clade comprised of more derived flying insect ligand-binding Ors, but, along with bristletail, firebrat and some mayfly Ors, are consistently resolved as a distinct set of genes that may constitute an evolutionary intermediate between gustatory receptors and the more derived Ors of flying insects. We propose to consider these \"primitive Ors\" separately from higher insect Ors until their cellular expression patterns and function are resolved and suggest a multistep evolutionary scenario ultimately leading to the highly sensitive, rapidly evolving and physiologically diverse Or gene family observed in higher insects.

evolutionary biology↗

Mutagenesis of orco impairs foraging but not oviposition in the hawkmoth Manduca sexta

Plant volatile detection through olfaction plays a crucial role in insect behaviors. In vivo, the odorant receptor co-receptor orco is an obligatory component for the function of odorant receptors (ORs), a major receptor family involved in insect olfaction. We used CRISPR-Cas9 targeted mutagenesis to knock-out (KO) orco in a neurophysiological model species, the hawkmoth Manduca sexta. M. sexta and its host, the Sacred Datura (Datura wrightii) share a model insect-plant relationship based on mutualistic and antagonistic life history traits. D. wrightii is the innately preferred nectar-source and oviposition host for M. sexta. Hence, the hawkmoth is an important pollinator while the M. sexta larvae are specialized herbivores of the plant. We generated an orco KO through CRISPR-Cas9 to test the consequences of a loss of OR-mediated olfaction in this insect-plant relationship. Neurophysiological characterization revealed severely reduced antennal and antennal lobe responses to representative odorants emitted by D. wrightii. In a wind-tunnel setting with a flowering plant, orco KO hawkmoths showed disrupted flight orientation and an ablated proboscis extension response to the natural stimulus. However, when testing the oviposition behavior of mated females encountering a non-flowering plant, there was no difference between orco KO and wild type females regarding upwind flight orientation and number of eggs laid. Overall, OR-mediated olfaction is essential for foraging and pollination behaviors, but plant-seeking and oviposition behaviors appear largely unaffected. Significance statementInsects detect plant volatiles mainly through the expression of ORs and IRs on the antennal olfactory sensory neurons (OSNs). In vivo, Orco is an obligate partner for OR, but not IR function and ORs mediate a vast spectrum of olfactory perception. We applied CRISPR-Cas9 in M. sexta to mutate the orco gene and determine the physiological and behavioral implication of a loss of Orco receptor function in a semi-ecological interaction with D. wrightii. We found that while behaviors related to foraging were largely disrupted, other sensory modalities outside Orco function determine the relationship between an ovipositing female and its plant host. These results have implications toward understanding the olfactory basis of insect-plant interactions shaping our ecological and agricultural landscapes.

neuroscience↗

Tissue embedding in a silica hydrogel for functional investigations

Embedding procedures can be challenging for delicate specimens. We present a method based on a sodium metasilicate (waterglass) gel to embed tissue samples for acute physiological studies. We show that the application of such a colloidal gel has minimal effects on the properties of buffered solutions and cell activity, allowing functional investigations on sensitive cells such as ciliated insect olfactory neurons.

neuroscience↗

The Drosophila pheromone Z4-11Al is encoded together with habitat olfactory cues and mediates species-specific communication

Mate recognition in animals evolves during niche adaptation and involves habitat and social olfactory signals. Drosophila melanogaster is attracted to fermenting fruit for feeding and egg-laying. We show that, in addition, female flies release a pheromone (Z)4-undecenal (Z4-11Al), that elicits flight attraction in both sexes. The biosynthetic precursor of Z4-11Al is the cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7,11-HD), which is known to afford reproductive isolation between D. melanogaster and D. simulans. A pair of alternatively spliced receptors, Or69aB and Or69aA, is tuned to Z4-11Al and to food olfactory cues, respectively. These receptors are co-expressed in the same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, long-range communication: the close relative D. simulans does not respond. That Or69aA and Or69aB have adopted dual olfactory traits highlights the interplay of habitat and social signals in mate finding. These olfactory receptor genes afford a collaboration between natural and sexual selection, which has the potential to drive phylogenetic divergence.

animal behavior and cognition↗