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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.

Brain wiring is remarkably precise, yet most neurons readily form synapses with incorrect partners when given the opportunity. Dynamic axon-dendritic positioning can restrict synaptogenic encounters, but the spatiotemporal interaction kinetics and their regulation remain essentially unknown inside developing brains. Here we show that the kinetics of axonal filopodia restrict synapse formation and partner choice for neurons that are not otherwise prevented from making incorrect synapses. Using 4D imaging in developing Drosophila brains, we show that filopodial kinetics are regulated by autophagy, a prevalent degradation mechanism whose role in brain development remains poorly understood. With surprising specificity, autophagosomes form in synaptogenic filopodia, followed by filopodial collapse. Altered autophagic degradation of synaptic building material quantitatively regulates synapse formation as shown by computational modeling and genetic experiments. Increased filopodial stability enables incorrect synaptic partnerships. Hence, filopodial autophagy restricts inappropriate partner choice through a process of kinetic exclusion that critically contributes to wiring specificity. The molecular mechanisms that restrict synapse formation with incorrect partners remain unclear. Here, authors use 4D imaging in developing Drosophila brains to show that filopodial kinetics are regulated by autophagy and this restricts inappropriate partner choice through a process of kinetic exclusion

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.

Over the past decade, several studies have demonstrated that idiosyncratic animal behaviors remain stable over long time periods. The stability of individually variable behaviors over time is often referred to as an animal's individuality, or personality. However, most experimental studies have focused on individuality in a single, well-defined environmental context, whereas it is well-established from population studies that animal behavior is highly context-dependent. The 'person-situation debate' in humans and decades of observations of animal individuality under intrinsically variable natural conditions raise the question of whether and to what extent animal behavior remains stable across different situations, such as changing environmental contexts. For instance, one individual might be generally more visually guided than another, or rely only on one particular visual cue, or even on this very cue only in a specific environmental context. Here, we use a combination of both well-established and novel behavioral assays to demonstrate the relationship between individual behavior and variable environmental context under tightly controlled laboratory conditions in the model system Drosophila melanogaster. The stability of three individual traits (termed exploration, attention, and anxiety) was investigated under changing environmental contexts (temperature, visual cues, arena shape), in both walking and flying flies. We find that individuality is highly context-dependent, but even under the most extreme environmental alterations tested, stability of behavior always persisted in at least one of the traits. Furthermore, our quantification reveals a hierarchical order of environmental features influencing individuality. In summary, our work demonstrates that, similar to humans, fly individuality persists across different contexts, and individual differences shape behavior across variable environments, thereby making the underlying developmental and functional mechanisms amenable to genetic dissection.Competing Interest StatementThe authors have declared no competing interest.Footnotes* We revised the manuscript to update and improve the text and to mainly improve the statistical modelling to obtain the data presented in the manuscript. All data has now been reanalized using a generalized linear model (GLM),

Active locomotion plays an important role in the life of many animals since it permits to explore the environment and find vital resources. Most insect species rely on a combination of visual cues such as celestial bodies, landmarks, or linearly polarized light to navigate or to 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 or shiny foil. Although multiple reports described different behavioral responses of various insects to such shiny surfaces, little is known about the retinal detectors or the underlying neural circuits. Our goal was to quantify the behavioral responses of free flying Drosophila melanogaster, a molecular genetic model organism that allows for systematic dissection of neural circuitry. Fruit flies were placed in a custom-built arena with controlled environmental parameters (temperature, humidity, and light intensity). Flight densities and landings were quantified for hydrated and dehydrated fly populations when separately exposed to three different stimuli such as a diffusely-reflecting matt plate, a small patch of shiny foil, versus real water. Our analysis reveals for the first time that flying fruit flies indeed use vision to guide their flight maneuvers around shiny surfaces.Competing Interest StatementThe authors have declared no competing interest.

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