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Many navigating insects include the celestial polarization pattern as an additional visual cue to orient their travels. Spontaneous orientation responses of both walking and flying fruit flies ( Drosophila melanogaster ) to linearly polarized light have previously been demonstrated. Using newly designed modular flight arenas consisting entirely of off-the-shelf parts and 3D-printed components we present individual flying flies with a slow and continuous rotational change in the incident angle of linear polarization. Under such open-loop conditions, single flies choose arbitrary headings with respect to the angle of polarized light and show a clear tendency to maintain those chosen headings for several minutes, thereby adjusting their course to the slow rotation of the incident stimulus. Importantly, flies show the tendency to maintain a chosen heading even when two individual test periods under a linearly polarized stimulus are interrupted by an epoch of unpolarized light lasting several minutes. Finally, we show that these behavioral responses are wavelength-specific, existing under polarized UV stimulus while being absent under polarized green light. Taken together, these findings provide further evidence supporting Drosophila’s abilities to use celestial cues for visually guided navigation and course correction.

Rab GTPases are molecular switches that regulate membrane trafficking in all cells. Neurons have particular demands on membrane trafficking and express numerous Rab GTPases of unknown function. Here, we report the generation and characterization of molecularly defined null mutants for all 26 rab genes in Drosophila . In flies, all rab genes are expressed in the nervous system where at least half exhibit particularly high levels compared to other tissues. Surprisingly, loss of any of these 13 nervous system-enriched Rabs yielded viable and fertile flies without obvious morphological defects. However, all 13 mutants differentially affected development when challenged with different temperatures, or neuronal function when challenged with continuous stimulation. We identified a synaptic maintenance defect following continuous stimulation for six mutants, including an autophagy-independent role of rab26. The complete mutant collection generated in this study provides a basis for further comprehensive studies of Rab GTPases during development and function in vivo.

Active locomotion plays an important role in the life of many animals, permitting them to explore the environment, find vital resources, and escape predators. Most insect species rely on a combination of visual cues such as celestial bodies, landmarks, or linearly polarized light to navigate or orient themselves in their surroundings. In nature, linearly polarized light can arise either from atmospheric scattering or from reflections off shiny non-metallic surfaces like water. Multiple reports have described different behavioral responses of various insects to such shiny surfaces. Our goal was to test whether free-flying Drosophila melanogaster, a molecular genetic model organism and behavioral generalist, also manifests specific behavioral responses when confronted with such polarized reflections. Fruit flies were placed in a custom-built arena with controlled environmental parameters (temperature, humidity, and light intensity). Flight detections and landings were quantified for three different stimuli: a diffusely reflecting matt plate, a small patch of shiny acetate film, and real water. We compared hydrated and dehydrated fly populations, since the state of hydration may change the motivation of flies to seek or avoid water. Our analysis reveals for the first time that flying fruit flies indeed use vision to avoid flying over shiny surfaces.

Animal behavior is individually variable, and this variability is often consistent over time, a phenomenon called individuality or personality when multiple traits are involved. However, most studies test individuality in only one environment, even though behavior is known to be context-dependent. Analogous to the human ‘person-situation debate,’ we asked whether and to what extent behavioral individuality persists across changing environmental situations in Drosophila melanogaster . Using established and new behavioral assays, we examined three individual traits, namely exploration, attention, and anxiety, across varying environmental contexts, including temperature, visual cues, and arena shape, in both walking and flying flies. We found that individuality is strongly context-dependent, but even under substantial environmental changes, at least one behavioral trait retained individual-specific variation. Different environmental features did not affect individuality equally; instead, they formed a hierarchy in their influence on behavioral consistency. This hierarchy was supported by generalized linear modeling and hierarchical linear mixed-model analysis. Our results show that, as in humans, individuality in flies persists across different situations, although less strongly than across repeated tests in the same context. These findings establish Drosophila as a model for dissecting the developmental, neural, and genetic mechanisms underlying consistent individual differences in behavior across variable environments.

Animal behavior is individually variable, and this variability is often consistent over time, a phenomenon called individuality or personality when multiple traits are involved. However, most studies test individuality in only one environment, even though behavior is known to be context-dependent. Analogous to the human ‘person-situation debate,’ we asked whether and to what extent behavioral individuality persists across changing environmental situations in Drosophila melanogaster . Using established and new behavioral assays, we examined three individual traits, namely exploration, attention, and anxiety, across varying environmental contexts, including temperature, visual cues, and arena shape, in both walking and flying flies. We found that individuality is strongly context-dependent, but even under substantial environmental changes, at least one behavioral trait retained individual-specific variation. Different environmental features did not affect individuality equally; instead, they formed a hierarchy in their influence on behavioral consistency. This hierarchy was supported by generalized linear modeling and hierarchical linear mixed-model analysis. Our results show that, as in humans, individuality in flies persists across different situations, although less strongly than across repeated tests in the same context. These findings establish Drosophila as a model for dissecting the developmental, neural, and genetic mechanisms underlying consistent individual differences in behavior across variable environments.

Many navigating insects include the celestial polarization pattern as an additional visual cue to orient their travels. Spontaneous orientation responses of both walking and flying fruit flies (Drosophila melanogaster) to linearly polarized light have previously been demonstrated. Using newly designed modular flight arenas consisting entirely of off-the-shelf parts and 3D-printed components we present individual flying flies with a slow and continuous rotational change in the incident angle of linear polarization. Under such open-loop conditions, single flies choose arbitrary headings with respect to the angle of polarized light and show a clear tendency to maintain those chosen headings for several minutes, thereby adjusting their course to the slow rotation of the incident stimulus. Importantly, flies show the tendency to maintain a chosen heading even when two individual test periods under a linearly polarized stimulus are interrupted by an epoch of unpolarized light lasting several minutes. Finally, we show that these behavioral responses are wavelength-specific, existing under polarized UV stimulus while being absent under polarized green light. Taken together, these findings provide further evidence supporting Drosophila's abilities to use celestial cues for visually guided navigation and course correction. Footnotes * https://www.flygen.org/skylight-navigation

The quantitative study of behavioral responses provides crucial information about how neural circuits process visual information, thereby revealing the computations responsible for shaping the animal's perception of the outside world. Over the last decade, insects have served as particularly powerful model systems, either when walking on air suspended balls (spherical treadmill), or when flying while glued to a needle (virtual flight arena). The use of virtual flight arenas is complicated by the fact that an effective experimental setup needs to combine a rather complex set of custom-built mechanical, electronic, and software components. Assembling such an apparatus amounts to a major challenge when working in an environment without the support of a machine shop. Here we present detailed instructions for the assembly of virtual flight arenas optimized for Drosophila skylight navigation, which can easily be modified towards other uses. This system consists entirely of off-the-shelf parts and 3D-printed components, combining a modular flight arena designed to reduce visual artifacts, swappable high-power LED light sources, polarization filters on a computer-controlled rotating filter wheel, all placed within a temperature and humidity controlled environment. Taken together, these findings demonstrate the usefulness of these assays for the study of skylight navigation in flies. Footnotes * https://www.flygen.org/skylight-navigation

In the fly optic lobe ~800 highly stereotypical columnar microcircuits are arranged retinotopically to process visual information. Differences in cellular composition and synaptic connectivity within functionally specialized columns remains largely unknown. Here we describe the cellular and synaptic architecture in medulla columns located downstream of photoreceptors in the 'dorsal rim area' (DRA), where linearly polarized skylight is detected for guiding orientation responses. We show that only in DRA medulla columns, both R7 and R8 photoreceptors target to the bona fide R7 target layer where they form connections with previously uncharacterized, modality-specific Dm neurons: Two morphologically distinct DRA-specific cell types (termed Dm-DRA1 and Dm-DRA2) stratify in separate sublayers and exclusively contact polarization-sensitive DRA inputs, while avoiding overlaps with color-sensitive Dm8 cells. Using the activity-dependent GRASP and trans-Tango techniques, we confirm that DRA R7 cells are synaptically connected to Dm-DRA1, whereas DRA R8 form synapses with Dm-DRA2. Finally, using live imaging of ingrowing pupal photoreceptor axons, we show that DRA R7 and R8 termini reach layer M6 sequentially, thus separating the establishment of different synaptic connectivity in time. We propose that a duplication of R7→Dm circuitry in DRA ommatidia serves as an ideal adaptation for detecting linearly polarized skylight using orthogonal e-vector analyzers.

Animals, including small insects, can explore complex natural environments to locate resources and potential mates. How a miniaturized nervous system extracts actionable structure from complex visual scenes to guide effective exploration remains incompletely understood. To bridge the gap between behavioristic experimental control and ethological realism, we combined a virtual-reality flight assay with naturalistic three-dimensional environments based on high-resolution satellite imagery of real-world landscapes. Flies that had never experienced natural environments exhibited individually stable, non-random exploration patterns and preferred flying over vegetated and elevated terrain while avoiding water-like features, indicative of a minimalistic world model for ecologically relevant terrain selection. Flight paths were characterized by saccadic turns, which we analyzed in relation to visual scene components, including brightness, color composition, optic flow, elevation, and contrast. Using multivariable regression modeling, we identified a hierarchy of visual cues influencing saccade frequency, amplitude, and directionality, and mapped the retinal areas most strongly gating saccadic decision-making. We discovered individual differences in motion-sensitivity thresholds that predict stable individual exploration-exploitation phenotypes. indicating a population-level bet-hedging strategy to increase terrain coverage and resource encounter rates. Individuality-based probabilistic decision-making simulations, utilizing our hierarchical visual models, successfully replicated exploration behavior, with the predicted dispersal and trajectory statistics matching the empirical data and demonstrating generality even for visual assays not included in the training dataset. Our work links individual visual decision rules to efficient exploration mechanisms of large-scale natural landscapes, potentially inspiring neural circuit theory, ecological prediction frameworks, vision-based pest control, and energy-efficient autonomous system design.Competing Interest StatementThe authors have declared no competing interest.Funder Information DeclaredDeutsche Forschungsgemeinschaft, LI 2640/1-1, FOR5289 LI 2640/2-1

Rab GTPases are molecular switches that regulate membrane trafficking in all cells. Neurons have particular demands on membrane trafficking and express numerous Rab GTPases of unknown function. Here we report the generation and characterization of molecularly defined null mutants for all 26 rab genes in Drosophila. In addition, we created a transgenic fly collection for the acute, synchronous release system RUSH for all 26 Rabs. In flies, all rab genes are expressed in the nervous system where at least half exhibit particularly high levels compared to other tissues. Surprisingly, loss of any of these 13 nervous-system enriched Rabs yields viable and fertile flies without obvious morphological defects. However, 9 of these 13 affect either developmental timing when challenged with different temperatures, or neuronal function when challenged with continuous stimulation. These defects are non-lethal under laboratory conditions, but represent sensitized genetic backgrounds that reveal limits of developmental and functional robustness to environmental challenges. Interestingly, the neuronal rab26 was previously proposed to function in synaptic maintenance by linking autophagy and synaptic vesicle recycling and we identified rab26 as one of six rab mutants with reduced synaptic function under continuous stimulation conditions. However, we found no changes to autophagy or synaptic vesicle markers in the rab26 mutant, but instead a cell-specific role in membrane receptor turnover associated with cholinergic synapses in the fly visual system. Our systematic functional analyses suggest that several Rabs ensure robust development and function under varying environmental conditions. The mutant and transgenic fly collections generated in this study provide a basis for further studies of Rabs during development and homeostasis in vivo.