Biology subjects

Hansson, B. S.

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

At least 19 recordsLinked to original sources

bioRxiv2024

Quantitive variation of male and female-specific compounds in 99 drosophilid flies

Variation in sex pheromones is regarded as one of the causes of reproductive isolation and speciation. We recently identified 51 male- and female-specific compounds - many of which function as sex pheromones - in 99 drosophilid species1. Here, we report that despite many of these compounds being shared between species, their quantities differ significantly. For example, although 34 drosophilid species share the male-specific compound cis-vaccenyl acetate (cVA), which plays a critical role in regulating various social and sexual behaviors, the amount of cVA can differ by up to 600-fold between different species. Additionally, we found 7-tricosene, the cuticular hydrocarbon pheromone, present in 35 Drosophila species. Our findings indicate that 7-tricosene is equally present in both sexes of 14 species, more abundant in males of 14 species, and more abundant in females of 7 species. We provide raw data on the concentration of potential pheromone components in the 99 drosophilids, which can provide important insights for further research on the behavior and evolution of these species. Quantitative variations highlight species-specific patterns, suggesting an additional mechanism for reproductive isolation built on specific combinations of compounds at set concentrations.

evolutionary biology↗

bioRxiv2024

Preference for and resistance to a toxic sulfur volatile opens up a unique niche in Drosophila busckii

The ability to tolerate otherwise toxic compounds can open up unique niches in nature. Among drosophilid flies few examples of such adaptations are known and then typically from highly host specific species. Here we show that the human commensal Drosophila busckii uses dimethyldisulfide (DMDS) as a key mediator in its host selection. Despite DMDSs neurotoxic properties1, D. busckii has evolved tolerance towards high concentrations and uses the compound as an olfactory cue to pinpoint food and oviposition sites. This adaptability is likely linked to an insensitive cytochrome c oxidase (COX), a DMDS target in other insects. Our findings position D. busckii as a potential model for studying resistance to toxic gases affecting COX and offer valuable insights into evolutionary adaptations within specific ecological contexts.

ecology↗

bioRxiv2024

Temperature-mediated dynamics: unraveling the impact of temperature on cuticular hydrocarbon profiles, mating behavior, and life history traits in three Drosophila species

In a world grappling with climate change, understanding the enduring impact of changes in temperature on insect adult traits is crucial. Here, we explored the intricate dynamics of exposure to different temperatures in three Drosophila species: Drosophila ezoana originating in Arctic regions, D. novamexicana in arid, hot environments, and in the cosmopolitan species D. virilis. Rearing these flies at 15, 20, 25, and 30{degrees}C revealed striking variations in their cuticular hydrocarbon (CHC) profiles, known to mediate mate recognition and prevent water loss in insects. The cold-adapted D. ezoana consistently exhibited reduced CHC levels with increasing temperatures, while the warm-adapted D. novamexicana and the cosmopolitan D. virilis displayed more nuanced responses. Additionally, we observed a significant influence of rearing temperature on the mating behavior of these flies, where those reared at the extreme tempreatures, 15 and 30{degrees}C, exhibiting reduced mating success. Consequently, this led to a decrease in the production of adult offspring. Also these adult offspring underwent notable alterations in life history traits, reaching adulthood more rapidly at 25 and 30{degrees}C but with lower weight and reduced longevity. Furthermore, among these offspring, those produced by the cold-adapted D. ezoana were more vulnerable to desiccation and starvation compared to those from the warm-adapted D. novamexicana and the cosmopolitan D. virilis. In summary, our research underscores the intricate interplay between temperature, ecological adaptation and various life history traits in Drosophila species from distinct agro-ecological regions. The observed variations in CHC profiles, mating behavior, fertility and responses to environmental stressors collectively provide valuable insights into how environmental conditions shape the biology and ecology of insects.

ecology↗

bioRxiv2023

Male cuticular pheromones stimulate removal of the mating plug and promote re-mating through pC1 neurons in Drosophila females

In birds and insects, the female uptakes sperm for a specific duration post-copulation known as the ejaculate holding period (EHP) before expelling unused sperm and the mating plug through sperm ejection. In this study, we found that Drosophila melanogaster females shortens the EHP when incubated with males or mated females shortly after the first mating. This phenomenon, which we termed male-induced EHP shortening (MIES), requires Or47b+ olfactory and ppk23+ gustatory neurons, activated by 2-methyltetracosane and 7-tricosene, respectively. These odorants raise cAMP levels in pC1 neurons, responsible for processing male courtship cues and regulating female mating receptivity. Elevated cAMP levels in pC1 neurons reduce EHP and reinstate their responsiveness to male courtship cues, promoting re-mating with faster sperm ejection. This study established MIES as a genetically tractable model of sexual plasticity with a conserved neural mechanism. Significance StatementSexual plasticity, the adaptation of reproductive behavior to social changes, was explored in the fruit fly, a genetically tractable model insect. Our findings revealed that inseminated females, encountering another courting male post-mating, shorten the ejaculate holding period (EHP). Specific olfactory and gustatory pathways regulating this phenomenon were identified, converging on the pC1 neurons in the brain-a conserved neural circuit that regulates female mating activity. Odors associated with EHP shortening increased the second messenger cAMP. The transient elevation of cAMP heightened the excitability of pC1 neurons, facilitating the prompt removal of the male ejaculate and subsequent re-mating . This study established a behavioral model of sexual plasticity and provided a framework for understanding the neural circuit processes involved.

neuroscience↗

bioRxiv2023

Olfactory learning modulates a neural circuit mediating innate odor-guided behavior in Drosophila

Behavior is often categorized as being innate or learned, with the specific circuits being assigned to one of these categories. In Drosophila, neural circuits mediating an innate behavioral response are considered as being "hard-wired", as activation of these neuronal pathways leads to stereotyped behaviors. However, only a limited number of studies assessed whether innate behaviors and their underlying neural circuits are plastic or show experience-dependent modulation. Here, we show that experience modulates second-order olfactory neurons involved in innate behavioral responses. We focus on the neural circuit defined by multiglomerular projection neurons (mPNs) that target the lateral horn, a structure relevant in the genesis of innate behavior. We show that mPNs, coding for odor attraction, are bidirectionally modulated after olfactory associative learning: when an olfactory stimulus is paired with an aversive electric shock, the activity of these neurons is decreased, while when the odor is paired with a sucrose-reward they are potentiated. We further show that this modulation requires glutamate and serotonin signaling, and that downstream third-order neurons are consequently affected. The bidirectional nature of the plasticity in these neurons is reflected in behavior: silencing mPN activity leads to odor avoidance, while artificial activation induces approach. While output from the mPNs is not required in aversive olfactory conditioning, silencing these neurons during retrieval of appetitive memories leads to a significant memory impairment. Artificially activating these neurons during odor presentation is sufficient to generate a 3 h appetitive memory. Our study in flies shows that a neural circuit coding for innate odor attraction can contribute to learned behavior, is modulated by olfactory learning and can provide reward-like reinforcement.

neuroscience↗

bioRxiv2023

Experience-dependent plasticity of a highly specific olfactory circuit in Drosophila melanogaster

Drosophila melanogaster encounters a variety of odor cues signaling potentially harmful threats through-out its life, which are detected by highly specialized olfactory circuits enabling the animal to avoid them. We studied whether such crucial neuronal pathways are hard-wired or can be modulated by experience. Using long-term exposure to high concentrations of geosmin, an indicator of potentially lethal microorganisms, we demonstrate at the single-cell level that the underlying neuronal circuitry undergoes structural changes in the antennal lobe, while higher brain centers remain unaffected. In particular, second-order neurons show neurite extensions and synaptic remodeling after the exposure period, whereas olfactory sensory neurons and glia cells remain unaffected. Flies that were exposed to geosmin tolerate this innately aversive odorant in general choice and oviposition assays. We show that even a highly specific olfactory circuit is plastic and adaptable to environmental changes. HIGHLIGHTSO_LIThe highly specific geosmin circuit is modulated by experience-dependent plasticity C_LIO_LIPN dendritic extensions cause a volumetric increase of the geosmin-detecting glomerulus C_LIO_LILNs are remodeled while OSNs and glia cells remain unaffected by long-term exposure C_LIO_LIFlies adapt their behavior to an odorant signaling a potential lethal threat C_LI

neuroscience↗

bioRxiv2023

Temperature-dependent modulation of odor-dependent behavior in three drosophilid fly species of differing thermal preference

Rapid and ongoing climate change increases global temperature and impacts both feeding and reproduction in insects. The sense of smell plays an important underlying role in these behaviors in most insect species. Here, we aimed to investigate how changing temperatures affect odor detection and ensuing behavior in three drosophilid flies: Drosophila novamexicana, D. virilis and D. ezoana, species that have adapted to life in desert, global and subarctic climates, respectively. Using a series of thermal preference assays, we confirmed that the three species indeed exhibit distinct temperature preferences. Next, using single sensillum recording technique, we classified olfactory sensory neurons (OSNs) present in basiconic sensilla on the antenna of the three species and thereby identified ligands for each OSN type. In a series of trap assays we proceeded to establish the behavioral valence of the best ligands and chose guaiacol, methyl salicylate and isopropyl benzoate as representatives of a repellent, attractant and neutral odor. Next, we assessed the behavioral valence of these three odors in all three species across a thermal range (10-35 C), with flies reared at 18{degrees}C and 25{degrees}C. We found that both developmental and experimental temperatures affected the behavioral performance of the flies. Our study thus reveals temperature-dependent changes in odor-guided behavior in drosophilid flies.

ecology↗

bioRxiv2022

Diversification of neuropil organization in specialized and broadly tuned olfactory glomerular circuits in Drosophila melanogaster

In the Drosophila olfactory system most odorants are encoded in the antennal lobe in a combinatory way, activating several glomerular circuits. However, odorants of particular ecological role for the fly are encoded through activation of a single specialized olfactory pathway. Comparative analyses of densely reconstructed connectomes of one broadly tuned glomerulus (DL5) and one narrowly tuned glomerulus (DA2) gained detailed insight into the variations of synaptic circuitries of glomeruli with different computational tasks. Our approach combined laser-branding of glomeruli of interest with volume based focused ion beam-scanning electron microscopy (FIB-SEM) to enable precise targeting and analysis of the two glomeruli. We discovered differences in their neuronal innervation, synaptic composition and specific circuit diagrams of their major cell types: olfactory sensory neurons (OSNs), uniglomerular projection neurons (uPNs) and multiglomerular neurons (MGNs). By comparing our data with a previously mapped narrowly tuned glomerulus (VA1v), we identified putative generic features of narrowly tuned glomerular circuits, including higher density of neuronal fibers and synapses, lower degree of OSN lateralization, stronger axo-axonic connections between OSNs, dendro-dendritic connections between many uPNs, and lower degree of presynaptic input on OSN axons. In addition, this work revealed that the dendrites of the single uPN in DL5 contain a substantial amount of autapses interconnecting distant regions of the dendritic tree. The comparative analysis of glomeruli allows to formulate synaptic motifs implemented in olfactory circuits with different computational demands.

neuroscience↗

bioRxiv2022

Increased ozone levels disrupt insect sexual communication

Insect sexual communication often relies upon sex pheromones1-3. Most insect pheromones, however, contain carbon-carbon double bonds and potentially degrade by oxidation4. Here, we show that already frequently reported increased levels of Anthropocenic ozone can oxidize all described male-specific pheromones of Drosophila melanogaster5-7, resulting in reduced amounts of e.g. cis-Vaccenyl Acetate and (Z)-7-Tricosene. At the same time female acceptance of ozone-exposed males is significantly delayed. Interestingly, groups of ozonized males also exhibit unnaturally high levels of male-male courtship behavior. When repeating similar experiments with nine other drosophilid species, we observe pheromone degradation and/or corrupted sex recognition in eight of them. Our data suggest that Anthropocenic levels of ozone can oxidize double bonds in a variety of insect pheromones extensively, thereby leading to deviations in sexual recognition.

animal behavior and cognition↗

bioRxiv2022

Aversive bimodal associations impact visual and olfactory memory performance in Drosophila

Insects rely heavily on sampling information from their environment for survival and fitness. Different sensory channels with dedicated downstream neural substrates are programmed to fine tune these signals and translate them into usable instructions to mediate complex behaviors. Sensory information can also be learned and stored as memories that influence decisions in the future. The learning of unimodal sensory signals, especially olfaction, has been studied extensively in different conditioning paradigms in different insects. Using the Drosophila melanogaster model in our work, we first investigated differences in the efficiencies of aversive associative visual and olfactory learning using sensory cues that are innately very attractive, such as blue or green light as well as food odors found in fruits or yeast. We then combined the presentation of visual and olfactory sensory stimuli during training to study the effect of bimodal integration on learning performance. When trained unimodally, flies did not easily learn visual stimuli, but when trained bimodally, they developed a significant short-term visual memory after a single learning trial. The bimodal training also suppressed the phototaxis response of the flies to near abolishment. However, a similar training did not enhance the short-term olfactory memory and in some cases, even caused reduction in strength. An enhancement after bimodal training was only seen with a weak long-term olfactory memory retrieved after 24h. Our study demonstrates that bimodal sensory integration is not always synergistic, but is conditional upon the training paradigm and inherent learning abilities of the sensory modalities involved.

animal behavior and cognition↗

bioRxiv2022

No functional contribution of the gustatory receptor, Gr64b, co-expressed in olfactory sensory neurons of Drosophila melanogaster

Chemosensation is essential for the survival of insects. Activities like searching for food, mating, and oviposition in the fruit fly, Drosophila melanogaster are to a great extent governed by chemical cues detected via olfaction and gustation. This chemical information is conveyed to higher brain centres via populations of diverse olfactory sensory neurons (OSNs) and gustatory sensory neurons (GSNs) expressing olfactory receptors (ORs) and gustatory receptors (GRs), respectively. ORs are exclusively expressed in the antenna and in the maxillary palps, while GRs are widely expressed in the labellum, tarsi, genitalia etc. Interestingly, 14 GRs were previously reported to be expressed in the antenna of D. melanogaster. However, the spatial expression pattern for all GRs and their functional role are still unclear. Recent data challenge the dogma that single OSNs express a single OR. In the present study, we studied the expression of 12 previously reported GRs among sensory structures on the fly antenna using the Gal4-UAS binary expression system. We observed antennal expression of nine out of the 12 reported. Out of these nine, consistent expression was only apparent for Gr64b, and we reconfirmed its presence in OSNs innervating three glomeruli in the antennal lobe. These glomeruli are known to be innervated by ab5A, ab5B and ab8A OSNs, respectively. Next, we generated double labelling crosses with Gr64b and observed co-expression of Gr64b with Or47a, which is expressed in the ab5B neuron. To elucidate the functional role of Gr64b co-expressed with Or47b, we challenged Or47a-expressing OSNs in wild type and Gr64b-/- mutant flies with odor stimulation using the single sensillum recording technique in two satiation states (fed and starved). Notably, we did not observe any significant odor sensitivity or specificity changes in Gr64b mutants as compared to wild type flies. Taken together, our results reveal co-expression of GRs with ORs in olfactory sensory neurons, while the functional contribution of the GR in this context remains obscure.

neuroscience↗

bioRxiv2022

Non-redundant odorant detection in a locust

Olfactory coding, from insects to humans, is canonically considered to involve considerable across-fiber coding already at the peripheral level, thereby allowing recognition of very large numbers of odor compounds. Here we show that the migratory locust, Locusta migratoria, has evolved an alternative strategy built on highly specific odorant receptors feeding into a complex primary processing center in the brain. By collecting odors from food and different life stages of the locust, we identified 208 ecologically relevant odorants, which we used to deorphanize 48 locust olfactory receptors via ectopic expression in Drosophila. Contrary to the often broadly tuned olfactory receptors of other insects, almost all locust receptors were found to be narrowly tuned to one ligand and most of these best ligands exclusively excited only one receptor. Knocking out a single receptor using CRISPR-Cas9 resulted in an abolished physiological and behavioral response to the corresponding ligand. We conclude that the locust olfactory system, with an apparent lack of redundancy among most olfactory receptors, differs from so-far described olfactory systems.

neuroscience↗

bioRxiv2022

Odorant receptor orthologues in conifer-feeding beetles display conserved responses to ecologically relevant odors

Insects are able to detect a plethora of olfactory cues using a divergent family of odorant receptors (ORs). Despite the divergent nature of this family, related species frequently express several evolutionarily conserved OR orthologues. In the largest order of insects, Coleoptera, it remains unknown whether OR orthologues have conserved or divergent functions in different species. Using HEK293 cells, we addressed this question through functional characterization of two groups of OR orthologues in three species of the Curculionidae (weevil) family, the conifer-feeding bark beetles Ips typographus L. ( Ityp) and Dendroctonus ponderosae Hopkins ( Dpon) (Scolytinae), and the pine weevil Hylobius abietis L. ( Habi; Molytinae). The ORs of H. abietis were annotated from antennal transcriptomes. Results show highly conserved response specificities, with one group of orthologues (HabiOR3/DponOR8/ItypOR6) responding exclusively to 2-phenylethanol (2-PE), and the other group (HabiOR4/DponOR9/ItypOR5) responding to angiosperm green leaf volatiles (GLVs). Both groups of orthologues belong to the coleopteran OR subfamily 2B, and share a common ancestor with OR5 in the cerambycid Megacyllene caryae, also tuned to 2-PE, suggesting a shared evolutionary history of 2-PE receptors across two beetle superfamilies. The detected compounds are ecologically relevant for conifer-feeding curculionids, and are probably linked to fitness, with GLVs being used to avoid angiosperm non-host plants, and 2-PE being important for intraspecific communication and/or playing a putative role in beetle-microbe symbioses. To our knowledge, this study is the first to reveal evolutionary conservation of OR functions across several beetle species and hence sheds new light on the functional evolution of insect ORs.

neuroscience↗

bioRxiv2022

Unique neural coding of crucial versus irrelevant plant odors in a hawkmoth

The sense of smell is pivotal for nocturnal moths to locate feeding and oviposition sites. However, these crucial resources are often rare and their bouquets are intermingled with volatiles emanating from surrounding background plants. Here we asked if the olfactory system of female hawkmoths, Manduca sexta, could differentiate between crucial and background cues. To answer this question, we collected nocturnal headspaces of numerous plants in a natural habitat of M. sexta. We analyzed the chemical composition of these headspaces, and used them as stimuli in physiological experiments at the antenna and in the brain. The intense odors of floral nectar sources evoked strong responses in virgin and mated female moths, most likely enabling the localization of profitable flowers at a distance. Bouquets of larval host plants and most background plants, in contrast, were subtle, thus potentially complicating host identification. However, despite being subtle, antennal responses and brain activation patterns evoked by the smell of larval host plants were clearly different from those evoked by other plants. Interestingly, this difference was even more pronounced in the antennal lobe of mated females, revealing a status-dependent tuning of their olfactory system towards oviposition sites. Our study suggests that female moths possess unique neural coding strategies to find not only conspicuous floral cues but also inconspicuous bouquets of larval host plants within a complex olfactory landscape.

neuroscience↗

bioRxiv2021

Response plasticity of Drosophila olfactory sensory neurons

In insect olfaction, sensitization refers to the amplification of a weak olfactory signal when the stimulus is repeated within a specific time window. In the vinegar fly, Drosophila melanogaster, his occurs already at the periphery, at the level of olfactory sensory neurons (OSNs) located in the antenna. In our study, we investigate whether sensitization is a widespread property in a set of seven types of OSNs, as well as the mechanisms involved. First, we characterize and compare differences in spontaneous activity, response velocity and response dynamics among the selected OSN types. These express different receptors with distinct tuning properties and behavioral relevance. Second, we show that sensitization is not a general property. Among our selected OSNs types, it occurs in those responding to more general food odors, while OSNs involved in very specific detection of highly specific ecological cues like pheromones and warning signals show no sensitization. Moreover, we show that mitochondria play an active role in sensitization by contributing to the increase in intracellular Ca2+ upon weak receptor activation. Thus, by using a combination of single sensillum recordings (SSR), calcium imaging and pharmacology, we widen the understanding of how the olfactory signal is processed at the periphery. O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

neuroscience↗

bioRxiv2021

Functional interaction between Drosophila olfactory sensory neurons and their support cells

Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g. by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.

neuroscience↗

bioRxiv2021

Higher-order olfactory neurons in the lateral horn supports odor valence and odor identity coding in Drosophila

Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster. We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We found that odors evoke reproducible, stereotypic and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons.

neuroscience↗

bioRxiv2021

Changes in antennal gene expression underlying sensory system maturation in Rhodnius prolixus

BackgroundTriatomine bugs are the blood feeding insect vectors transmitting Chagas disease to humans, a neglected tropical disease that affects over 8 million people, mainly in Latin America. The behavioral responses to host cues and bug signals in Rhodnius prolixus are state dependent, i.e., they vary as a function of post-ecdysis age. At the molecular level, these changes in behavior are probably due to a modulation of peripheral and central processes. In the present study, we report a significant modulation of the expression of a large set of sensory-related genes. Results were generated by means of antennal transcriptomes of 5th instar larvae along the first week (days 0, 2, 4, 6 and 8) after ecdysis sequenced using the Illumina platform. ResultsAge induced significant changes in transcript abundance were established in more than 6,120 genes (54,7 % of 11,186 genes expressed) in the R. prolixus antenna. This was especially true between the first two days after ecdysis when more than 2,500 genes had their expression significantly altered. In contrast, expression profiles were almost identical between day 6 and 8, with only a few genes showing significant modulation of their expression. A total of 86 sensory receptors, odorant carriers and odorant degrading enzymes were significantly modulated across age points and clustered into three distinct expression profiles. ConclusionsThe set of sensory genes whose expression increased with age (profile 3) may include candidates underlying the increased responsiveness to host cues shown by R. prolixus during the first days after molting. For the first time, we describe the maturation process undergone at the molecular level by the peripheral sensory system is described in an hemimetabolous insect.

molecular biology↗