@article {164000, title = {Odor tracking in insects: a multisensory behavior.}, journal = {J Exp Biol}, volume = {229}, year = {2026}, month = {2026 Feb 15}, abstract = {

Insects rely on sophisticated odor-tracking mechanisms to locate mates and food sources, or follow conspecific trails, in both two (e.g. substrate-based tracking by ants and termites) and three (e.g. airborne pheromone plume tracking by flying insects) dimensions. These behaviors rely on the integration of multisensory information and understanding them requires us to draw upon principles from odor transport physics, odor chemistry and sensory ecology. Airborne odor plumes are typically heterogeneous and turbulent, delivering chemical cues in intermittent bursts, while ground-based odor trails are more stable and localized. Hence, insects employ fundamentally distinct strategies to navigate these environments, shaped by the physical and chemical properties of the odorants. Insect odor-tracking behavior is mediated by an array of sensory modalities, including chemosensory, visual, mechanosensory and thermal inputs. Experimental approaches in both laboratory and field settings have revealed how insects integrate these cues to successfully identify odor sources under complex environmental conditions. Comparative studies, such as those examining diurnal versus nocturnal tracking, highlight how sensory prioritization shifts with ecological context, revealing adaptive neural integration mechanisms. This article reviews the behavioral strategies insects use for odor tracking in air and on the ground, focusing on the role of multisensory integration and the vulnerability of these behaviors to sensory noise. Emerging research on environmental disruptions, such as artificial light at night and air pollution, highlights the ecological threats to odor-mediated behaviors. By synthesizing insights from diverse insect taxa, we examine how sensory noise and anthropogenic change can impair essential behaviors such as foraging and mating.

}, keywords = {Animals, Behavior, Animal, Cues, Insecta, Odorants, Smell}, issn = {1477-9145}, doi = {10.1242/jeb.250945}, url = {https://pubmed.ncbi.nlm.nih.gov/41668668/}, author = {Soman, Shuchita and Ramaswamy, Sree Subha and Sane, Sanjay P} } @article {163999, title = {Sensory biology in a changing world: multisensory systems and interdisciplinary collaboration.}, journal = {J Exp Biol}, volume = {229}, year = {2026}, month = {2026 Feb 15}, abstract = {

Animals have evolved multiple sensory systems that can acquire environmental information guiding their behaviour, allowing them to adapt physiological parameters to current conditions. However, over the past century, anthropogenic changes have increasingly made information on environmental conditions less reliable, by introducing novel elements (such as synthetic chemicals or artificial light), by altering environmental parameters such as temperature, and by introducing fluctuations. Animals using multimodal information perceived through multiple senses may be more resilient to changes, as they can adjust their sensory strategy, giving more weight to information channels that are less disturbed than others. In this Commentary, we propose that to better understand how animals are affected by disturbed access to sensory information that is caused by anthropogenic influences, sensory biologists need to study all developmental stages of a wide range of species, and include entire ecosystems in their thinking. Comparative, interdisciplinary studies will be increasingly important if we are to understand and mitigate the sensory consequences of anthropogenic changes for animals.

}, keywords = {Animals, Ecosystem, Interdisciplinary Communication, Sensation}, issn = {1477-9145}, doi = {10.1242/jeb.251786}, url = {https://pubmed.ncbi.nlm.nih.gov/41668653/}, author = {Kelber, Almut and Gilmour, Kathleen M and Sane, Sanjay P} } @article {155511, title = {Encoding of antennal position and velocity by the Johnston{\textquoteright}s organ in hawkmoths.}, journal = {J Exp Biol}, year = {2025}, month = {2025 Mar 18}, abstract = {

Insect antennae function as versatile, multimodal sensory probes in diverse behavioural contexts. In addition to their primary role as olfactory organs, they serve essential mechanosensory functions across insects, including auditory perception, vestibular feedback, airflow detection, gravity sensing, and tactile sensation. These diverse functions are facilitated by the mechanosensory Johnston{\textquoteright}s organ (JO), located at the joint between the flagellum and the second antennal segment i.e. the pedicel. The pedicel-flagellum joint lacks muscles which means that the Johnston{\textquoteright}s organs can perceive only passive deflections of the flagellum. Earlier work which characterized the sensitivity and short response time of the sensory units of JO in hawkmoths, showed that their sensitivity to a broad frequency range is range-fractionated. This vastly expands the functional repertoire of the JO. However, it is not clear what components of antennal kinematics are encoded by the JO. Here, we conducted experiments to test the hypothesis that JO neurons encode the position and velocity of angular movements of the flagellum. We recorded intracellularly from the axons of primary sensory neurons of JO while stimulating it with ramp-and-hold stimuli in which either the antennal position or the antennal angular velocity was maintained at various constant values. Our study shows that JO neurons encode angular velocity and position of the antenna in their response. We also characterized the neural adaptation of the responses to angular velocities and positions. A majority of neurons were sensitive to a movement in the ventrad direction, in the direction of gravity. The adaptation and the directional response properties give rise to a nonlinear hysteresis-like response. Together, these findings highlight the neurophysiological basis underlying the functional versatility of the JO.

}, keywords = {Daphnis nerii; Adaptation; Hawkmoths; Hysteresis; Johnston{\textquoteright}s organ; Mechanosensors; Neurophysiology; Sensory encoding.}, issn = {1477-9145}, doi = {10.1242/jeb.249342}, url = {https://pubmed.ncbi.nlm.nih.gov/40099381/}, author = {Mukunda, Chinmayee L and Sane, Sanjay P} } @article {161984, title = {Mechanosensory cephalic bristles mediate rapid flight initiation in hawkmoths.}, journal = {J Comp Physiol A Neuroethol Sens Neural Behav Physiol}, year = {2025}, month = {2025 Oct 31}, abstract = {

Endothermic insects including bees, butterflies, and moths need to warm up their flight muscles before taking flight. For instance, diurnal butterflies bask in the sun to heat their flight muscles, whereas nocturnal hawkmoths display a pre-flight shivering behavior in which small-amplitude wing movements cause flight muscles to warm up, eventually generating large-amplitude wing motion for flight. The time required for warm-up puts such insects at considerable risk if they need to rapidly escape from predators. Here, we show that upon experiencing a sudden air-puff on the head, hawkmoths with lower thoracic temperatures can rapidly initiate flight without the need for pre-flight shivering. This response is mediated by mechanosensory cephalic bristles that are located beneath the scales on their head. When activated, these bristles trigger a set of flight-related reflexes including antennal positioning, foreleg extension, wing movement, and abdominal flexion. Some of the mechanosensory neurons associated with the cephalic bristles arborize in the subesophageal zone (SEZ) and antennal motor and mechanonsensory centre (AMMC), whereas most arborize in pro-, meso- and meta-thoracic ganglia, which contain the motor circuitry for foreleg motion, flight, and abdominal flexion. Thermal recordings revealed that large-amplitude flapping following cephalic bristle-stimulation occurs at lower thoracic temperatures than required for endogenously-initiated take off. Electromyogram recordings from steering and indirect flight muscles show significant variability in activation latency in response to cephalic bristle stimuli. The range of latency values among different muscles overlaps, suggesting that cephalic bristle stimulation broadly activates indirect flight and steering muscles, thereby generating high-amplitude wing movement at lower thoracic temperatures. Thus, akin to locusts, the cephalic bristle system in hawkmoths rapidly triggers flight upon sensing danger, ensuring swift escape from potential threats.

}, keywords = {Daphnis nerii; Cephalic bristles; Endothermy; Flight reflexes; Hawkmoths; Insect flight; Pre-flight shivering}, issn = {1432-1351}, doi = {10.1007/s00359-025-01762-5}, author = {Manjunath, Maitri and Sane, Sanjay P} } @article {154147, title = {Structure of the Femoral Chordotonal Organ in the Oleander Hawkmoth, Daphnis nerii.}, journal = {The Journal of Comparative Neurology}, volume = {533}, year = {2025}, month = {2025 Feb}, pages = {e70022}, abstract = {

Insect legs serve as crucial organs for locomotion and also act as sensory probes into the environment. They are involved in several complex movements including walking, jumping, prey capture, manipulation of objects, and self-grooming. These behaviors require continuous modulation of motor output through mechanosensory feedback, which is provided by numerous mechanosensors located on the cuticle and within the soft tissue. A key mechanosensory organ in the insect leg, the femoral chordotonal organ (FeCO), detects movements of the femoro-tibial joint. This organ is multifunctional and senses both self-generated movements (proprioception) and external stimuli (exteroception). Movements of the tibia alter the length of FeCO, which activates the embedded mechanosensory neurons. Due to the mechanical nature of these stimuli, the structure and material properties of the FeCO are crucial for their function, alongside the encoding properties of FeCO neurons. Here, as a first step toward understanding how its structure modulates its function, we characterized the morphology and anatomy of FeCO in the hawkmoth Daphnis nerii. Using a combination of computed micro-tomography, neuronal dye fills, and confocal microscopy, we describe the structure of FeCO and the location, composition, and central projections of FeCO neurons. FeCO is located in the proximal half of the femur and is composed of the ventral (vFeCO) and dorsal scoloparia (dFeCO), which vary vastly in their sizes and in the number of neurons they house. Moreover, the characteristic accessory structures of chordotonal organs, the scolopales, significantly differ in their sizes when compared between the two scoloparia. FeCO neurons project to the central nervous system and terminate in the respective hemiganglia. Using these morphological data, we propose a mechanical model of FeCO, which can help us understand several FeCO properties relating to its physiological function.

}, keywords = {FeCO model; femoral chordotonal organs; femoro-tibial joint; mechanosensors; oleander hawkmoth Daphnis nerii; proprioception.}, issn = {1096-9861}, doi = {10.1002/cne.70022}, url = {https://pubmed.ncbi.nlm.nih.gov/39935029/}, author = {Virdi, Simran and Sane, Sanjay P} } @article {145430, title = {Generating controlled gust perturbations using vortex rings.}, journal = {PLoS One}, volume = {19}, year = {2024}, month = {2024}, pages = {e0305084}, abstract = {

To understand the locomotory mechanisms of flying and swimming animals, it is often necessary to develop assays that enable us to measure their responses to external gust perturbations. Typically, such measurements have been carried out using a variety of gusts which are difficult to control or characterize owing to their inherently turbulent nature. Here, we present a method of generating discrete gusts under controlled laboratory conditions in the form of a vortex rings which are well-characterized and highly controllable. We also provide the theoretical guidelines underlying the design of gust generators for specific applications. As a case study, we tested the efficacy of this method to study the flight response of freely-flying soldier flies Hermetia illucens. The vortex ring based method can be used to generate controlled gusts to study diverse phenomena ranging from a natural flight in insects to the artificial flight of insect-sized drones and micro-aerial vehicles.

}, keywords = {Animals, Diptera, Flight, Animal, Swimming}, issn = {1932-6203}, doi = {10.1371/journal.pone.0305084}, author = {Gupta, Dipendra and Sane, Sanjay P and Arakeri, Jaywant H} } @article {145432, title = {Insect Flight: State of the Field and Future Directions.}, journal = {Integr Comp Biol}, year = {2024}, month = {2024 Jul 09}, abstract = {

The evolution of flight in an early winged insect ancestral lineage is recognized as a key adaptation explaining the unparalleled success and diversification of insects. Subsequent transitions and modifications to flight machinery, including secondary reductions and losses, also play a central role in shaping the impacts of insects on broadscale geographic and ecological processes and patterns in the present and future. Given the importance of insect flight, there has been a centuries-long history of research and debate on the evolutionary origins and biological mechanisms of flight. Here, we revisit this history from an interdisciplinary perspective, discussing recent discoveries regarding the developmental origins, physiology, biomechanics, and neurobiology and sensory control of flight in a diverse set of insect models. We also identify major outstanding questions yet to be addressed and provide recommendations for overcoming current methodological challenges faced when studying insect flight, which will allow the field to continue to move forward in new and exciting directions. By integrating mechanistic work into ecological and evolutionary contexts, we hope that this synthesis promotes and stimulates new interdisciplinary research efforts necessary to close the many existing gaps about the causes and consequences of insect flight evolution.

}, issn = {1557-7023}, doi = {10.1093/icb/icae106}, author = {Treidel, Lisa A and Deem, Kevin D and Salcedo, Mary K and Dickinson, Michael H and Bruce, Heather S and Darveau, Charles-A and Dickerson, Bradley H and Ellers, Olaf and Glass, Jordan R and Gordon, Caleb M and Harrison, Jon F and Hedrick, Tyson L and Johnson, Meredith G and Lebenzon, Jacqueline E and Marden, James H and Niitep{\~o}ld, Kristjan and Sane, Sanjay P and Sponberg, Simon and Talal, Stav and Williams, Caroline M and Wold, Ethan S} } @article {140643, title = {The motor apparatus of head movements in the Oleander hawkmoth (Daphnis nerii, Lepidoptera).}, journal = {J Comp Neurol}, volume = {532}, year = {2024}, month = {2024 Jan}, pages = {e25577}, abstract = {

Head movements of insects play a vital role in diverse locomotory behaviors including flying and walking. Because insect eyes move minimally within their sockets, their head movements are essential to reduce visual blur and maintain a stable gaze. As in most vertebrates, gaze stabilization behavior in insects requires the integration of both visual and mechanosensory feedback by the neck motor neurons. Although visual feedback is derived from the optic flow over the retina of their compound eyes, mechanosensory feedback is derived from their organs of balance, similar to the vestibular system in vertebrates. In Diptera, vestibular feedback is derived from the halteres-modified hindwings that evolved into mechanosensory organs-and is integrated with visual feedback to actuate compensatory head movements. However, non-Dipteran insects, including Lepidoptera, lack halteres. In these insects, vestibular feedback is obtained from the antennal Johnston{\textquoteright}s organs but it is not well-understood how it integrates with visual feedback during head movements. Indeed, although head movements are well-studied in flies, the underlying motor apparatus in non-Dipteran taxa has received relatively less attention. As a first step toward understanding compensatory head movements in the Oleander hawkmoth Daphnis nerii, we image the anatomy and architecture of their neck joint sclerites and muscles using X-ray microtomography, and the associated motor neurons using fluorescent dye fills and confocal microscopy. Based on these morphological data, we propose testable hypotheses about the putative function of specific neck muscles during head movements, which can shed light on their role in neck movements and gaze stabilization.

}, keywords = {Animals, Dendritic Spines, Eye, Head Movements, Moths, Nerium}, issn = {1096-9861}, doi = {10.1002/cne.25577}, author = {Prusty, Agnish D and Sane, Sanjay P} } @article {139057, title = {Multisensory integration in insect flight control.}, journal = {Biol Lett}, volume = {20}, year = {2024}, month = {2024 Jan}, pages = {20230565}, keywords = {Animals, Insecta}, issn = {1744-957X}, doi = {10.1098/rsbl.2023.0565}, author = {Sane, Sanjay P and Wehling, Ric and Daniel, Tom} } @article {137344, title = {Through the looking glass: attempting to predict future opportunities and challenges in experimental biology.}, journal = {J Exp Biol}, volume = {226}, year = {2023}, month = {2023 Dec 15}, abstract = {

To celebrate its centenary year, Journal of Experimental Biology (JEB) commissioned a collection of articles examining the past, present and future of experimental biology. This Commentary closes the collection by considering the important research opportunities and challenges that await us in the future. We expect that researchers will harness the power of technological advances, such as {\textquoteright}-omics{\textquoteright} and gene editing, to probe resistance and resilience to environmental change as well as other organismal responses. The capacity to handle large data sets will allow high-resolution data to be collected for individual animals and to understand population, species and community responses. The availability of large data sets will also place greater emphasis on approaches such as modeling and simulations. Finally, the increasing sophistication of biologgers will allow more comprehensive data to be collected for individual animals in the wild. Collectively, these approaches will provide an unprecedented understanding of {\textquoteright}how animals work{\textquoteright} as well as keys to safeguarding animals at a time when anthropogenic activities are degrading the natural environment.

}, keywords = {Animals, Environment, Genomics}, issn = {1477-9145}, doi = {10.1242/jeb.246921}, author = {Gilmour, Kathleen M and Daley, Monica A and Egginton, Stuart and Kelber, Almut and McHenry, Matthew J and Patek, Sheila N and Sane, Sanjay P and Schulte, Patricia M and Terblanche, John S and Wright, Patricia A and Franklin, Craig E} } @article {129165, title = {Vestibular feedback for flight control in hawkmoths.}, journal = {Trends Neurosci}, year = {2023}, month = {2023 May 26}, abstract = {

Flying insects require mechanosensory feedback to rapidly generate compensatory responses to unexpected perturbations. Such feedback is critical in insects such as moths, which fly under low light levels, compromising their ability to visually compensate for aerial perturbations. Here, we describe how diverse mechanosensory organs have adapted to provide vestibular feedback in various insects, with particular focus on hawkmoths.

}, issn = {1878-108X}, doi = {10.1016/j.tins.2023.05.004}, author = {Sane, Sanjay P and Manjunath, Maitri and Mukunda, Chinmayee L} } @article {112956, title = {Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths.}, journal = {Elife}, volume = {11}, year = {2022}, month = {2022 Jun 27}, abstract = {

During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely-flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth , compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization primarily at low frequencies of body roll. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements at high of body roll.

}, issn = {2050-084X}, doi = {10.7554/eLife.78410}, author = {Chatterjee, Payel and Prusty, Agnish Dev and Mohan, Umesh and Sane, Sanjay P} } @article {119609, title = {Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths.}, journal = {Biol Lett}, volume = {18}, year = {2022}, month = {2022 Nov}, pages = {20220199}, abstract = {

In flying insects, head stabilization is an essential reflex that helps to reduce motion blur during fast aerial manoeuvres. This reflex is multimodal and requires the integration of visual and antennal mechanosensory feedback in hawkmoths, each operating as a negative-feedback-control loop. As in any negative-feedback system, the head stabilization system possesses inherent oscillatory dynamics that depend on the rate at which the sensorimotor components of the reflex operate. Consistent with this expectation, we\ observed small-amplitude oscillations in the head motion (or head wobble) of the oleander hawkmoth, which are accentuated when sensory feedback is aberrant. Here, we show that these oscillations emerge from the inherent dynamics of the multimodal reflex underlying gaze stabilization, and that the amplitude of head wobble is a function of both the visual feedback and antennal mechanosensory feedback from the Johnston{\textquoteright}s organs. Our data support the hypothesis that head wobble results from a multimodal, dynamically stabilized reflex loop that mediates head positioning.

}, keywords = {Animals, Arthropod Antennae, Flight, Animal, Head, Manduca, Moths, Reflex}, issn = {1744-957X}, doi = {10.1098/rsbl.2022.0199}, author = {Chatterjee, Payel and Mohan, Umesh and Sane, Sanjay P} } @article {88401, title = {Evidence for facultative migratory flight behavior in Helicoverpa armigera (Noctuidae: Lepidoptera) in India.}, journal = {PLoS One}, volume = {16}, year = {2021}, month = {2021}, pages = {e0245665}, abstract = {

Despite its deleterious impact on farming and agriculture, the physiology and energetics of insect migration is poorly understood due to our inability to track their individual movements in the field. Many insects, e.g. monarch butterflies, Danaus plexippus (L.), are facultative migrants. Hence, it is important to establish whether specific insect populations in particular areas migrate. The polyphagous insect, Helicoverpa armigera (H{\"u}bner), is especially interesting in this regard due to its impact on a variety of crops. Here, we used a laboratory-based flight mill assay to show that Helicoverpa armigera populations clearly demonstrate facultative migration in South India. Based on various flight parameters, we categorized male and female moths as long, medium or short distance fliers. A significant proportion of moths exhibited long-distance flight behavior covering more than 10 km in a single night, averaging about 8 flight hours constituting 61\% flight time in the test period. The maximum and average flight speeds of these long fliers were greater than in the other categories. Flight activity across sexes also varied; male moths exhibited better performance than female moths. Wing morphometric parameters including forewing length, wing loading, and wing aspect ratio were key in influencing long-distance flight. Whereas forewing length positively correlated with flight distance and duration, wing loading was negatively correlated.

}, issn = {1932-6203}, doi = {10.1371/journal.pone.0245665}, author = {Jyothi, Patil and Aralimarad, Prabhuraj and Wali, Vijaya and Dave, Shivansh and Bheemanna, M and Ashoka, J and Shivayogiyappa, Patil and Lim, Ka S and Chapman, Jason W and Sane, Sanjay P} } @article {102566, title = {Wings and halteres act as coupled dual-oscillators in flies.}, journal = {Elife}, volume = {10}, year = {2021}, month = {2021 Nov 16}, abstract = {

The mechanics of Dipteran thorax is dictated by a network of exoskeletal linkages which, when deformed by the flight muscles, generate coordinated wing movements. In Diptera, the forewings power flight, whereas the hindwings have evolved into specialized structures called halteres which provide rapid mechanosensory feedback for flight stabilization. Although actuated by independent muscles, wing and haltere motion is precisely phase-coordinated at high frequencies. Because wingbeat frequency is a product of wing-thorax resonance, any wear-and-tear of wings or thorax should impair flight ability. How robust is the Dipteran flight system against such perturbations? Here, we show that wings and halteres are independently-driven, coupled oscillators. We systematically reduced the wing length in flies and observed how wing-haltere synchronization was affected. The wing-wing system is a strongly-coupled oscillator, whereas the wing-haltere system is weakly-coupled through mechanical linkages which synchronize phase and frequency. Wing-haltere link acts in a unidirectional manner; altering wingbeat frequency affects haltere frequency, but not vice-versa. Exoskeletal linkages are thus key morphological features of the Dipteran thorax which ensure wing-haltere synchrony, despite severe wing damage.

}, issn = {2050-084X}, doi = {10.7554/eLife.53824}, author = {Deora, Tanvi and Sane, Siddharth S and Sane, Sanjay P} } @article {86829, title = {Editorial overview: Insect-inspired engineering: mechanisms, processes and algorithms.}, journal = {Curr Opin Insect Sci}, volume = {42}, year = {2020}, month = {2020 Dec}, pages = {vi-viii}, issn = {2214-5753}, doi = {10.1016/j.cois.2020.11.012}, author = {Sane, Sanjay P} } @article {83640, title = {Enhancing insect flight research with a lab-on-cables.}, journal = {Sci Robot}, volume = {5}, year = {2020}, month = {2020 Aug 26}, abstract = {

A cable-driven robot that tracks flying insects at close range offers a useful method to study insects in free flight.

}, issn = {2470-9476}, doi = {10.1126/scirobotics.abd7941}, author = {Sane, Sanjay P} } @article {78109, title = {Evolutionary constraints on flicker fusion frequency in Lepidoptera.}, journal = {J Comp Physiol A Neuroethol Sens Neural Behav Physiol}, year = {2020}, month = {2020 Jun 11}, abstract = {

Flying insects occupy both diurnal and nocturnal niches, and their visual systems encounter distinct challenges in both conditions. Visual adaptations, such as superposition eyes of moths, enhance sensitivity to low light levels but trade off with spatial and temporal resolution. Conversely, apposition eyes of butterflies enable high spatial resolution but are poorly sensitive in dim light. Although diel activity patterns of insects influence visual processing, their role in evolution of visual systems is relatively unexplored. Lepidopteran insects present an excellent system to study how diel activity patterns and phylogenetic position influence the visual transduction system. We addressed this question by comparing electroretinography measurements of temporal response profiles of diverse Lepidoptera to light stimuli that were flickering at different frequencies. Our data show that the eyes of diurnal butterflies are sensitive to visual stimuli of higher temporal frequencies than nocturnal moths. Hesperiid skippers, which are typically diurnal or crepuscular, exhibit intermediate phenotypes with peak sensitivity across broader frequency range. Across all groups, species within families exhibited similar phenotypes irrespective of diel activity. Thus, Lepidopteran photoreceptors may have diversified under phylogenetic constraints, and shifts in their sensitivity to higher temporal frequencies occurred concomitantly with the evolution of diurnal lifestyles.

}, issn = {1432-1351}, doi = {10.1007/s00359-020-01429-3}, author = {Chatterjee, Payel and Mohan, Umesh and Krishnan, Anand and Sane, Sanjay P} } @article {81507, title = {Insect architecture: structural diversity and behavioral principles.}, journal = {Curr Opin Insect Sci}, year = {2020}, month = {2020 Aug 22}, abstract = {

Insects build myriad structures out of diverse materials. These structures serve purposes that range from facilitating prey capture to housing their entire colony. Whereas some insects operate solitarily, others collectively build large and complex structures. The architecture of these structures vis-{\`a}-vis their ultimate function poses fascinating questions that require multidisciplinary investigations. Importantly, because the underlying design and architectural principles have evolved over millions of years to withstand multitude of environmental perturbations, they offer important lessons for human-made structures. The vast variety of insect-built structures reflects how diverse insects have adapted to resolve the ecological challenges in their specific habitats. Here, we survey insect-built structures from a comparative perspective to ask what design and architectural principles can be gleaned from them. We discuss the key hypotheses about building-behaviours, their neural underpinnings, the functional role of insect-built structures and their biomimetic potential.

}, issn = {2214-5753}, doi = {10.1016/j.cois.2020.08.005}, author = {Sane, Sanjay P and Ramaswamy, Sree Subha and Raja, Sreekrishna Varma} } @article {51001, title = {Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons.}, journal = {Curr Biol}, volume = {29}, year = {2019}, month = {2019 Jan 21}, pages = {283-293.e5}, abstract = {

Insect flight is a complex behavior that requires the integration of multiple sensory inputs with flight motor output. Although previous genetic studies identified central brain monoaminergic neurons that modulate Drosophila flight, neuro-modulatory circuits underlying sustained flight bouts remain unexplored. Certain classes of dopaminergic and octopaminergic neurons that project to the mushroom body, a higher integrating center in the insect brain, are known to modify neuronal output based on contextual cues and thereby organismal behavior. This study focuses on how monoaminergic modulation of mushroom body GABAergic output neurons (MBONs) regulates the duration of flight bouts. Octopaminergic neurons in the sub-esophageal zone stimulate central dopaminergic neurons (protocerebral anterior medial, PAM) that project to GABAergic MBONs. Either inhibition of octopaminergic and dopaminergic neurons or activation of GABAergic MBONs reduces the duration of flight bouts. Moreover, activity in the PAM neurons inhibits the GABAergic MBONs. Our data suggest that disinhibition of the identified neural circuit very likely occurs after flight initiation and is required to maintain the "flight state" when searching for distant sites, possibly related to food sources, mating partners, or a suitable egg-laying site. VIDEO ABSTRACT.

}, issn = {1879-0445}, doi = {10.1016/j.cub.2018.11.070}, author = {Manjila, Steffy B and Kuruvilla, Maria and Ferveur, Jean-Fran{\c c}ois and Sane, Sanjay P and Hasan, Gaiti} } @article {67830, title = {Flies land upside down on a ceiling using rapid visually mediated rotational maneuvers.}, journal = {Sci Adv}, volume = {5}, year = {2019}, month = {2019 Oct}, pages = {eaax1877}, abstract = {

Flies and other insects routinely land upside down on a ceiling. These inverted landing maneuvers are among the most remarkable aerobatic feats, yet the full range of these behaviors and their underlying sensorimotor processes remain largely unknown. Here, we report that successful inverted landing in flies involves a serial sequence of well-coordinated behavioral modules, consisting of an initial upward acceleration followed by rapid body rotation and leg extension, before terminating with a leg-assisted body swing pivoted around legs firmly attached to the ceiling. Statistical analyses suggest that rotational maneuvers are triggered when flies{\textquoteright} relative retinal expansion velocity reaches a threshold. Also, flies exhibit highly variable pitch and roll rates, which are strongly correlated to and likely mediated by multiple sensory cues. When flying with higher forward or lower upward velocities, flies decrease the pitch rate but increase the degree of leg-assisted swing, thereby leveraging the transfer of body linear momentum.

}, issn = {2375-2548}, doi = {10.1126/sciadv.aax1877}, author = {Liu, Pan and Sane, Sanjay P and Mongeau, Jean-Michel and Zhao, Jianguo and Cheng, Bo} } @article {62917, title = {Landing maneuvers of houseflies on vertical and inverted surfaces.}, journal = {PLoS One}, volume = {14}, year = {2019}, month = {2019}, pages = {e0219861}, abstract = {

Landing maneuvers of flies are complex behaviors which can be conceptually decomposed into sequences of modular actions, including body-deceleration, leg-extension, and body rotations. These behavioral {\textquoteright}modules{\textquoteright} must be coordinated to ensure well-controlled landing. The composite nature of these behaviors induces kinematic variability, making it difficult to identify the central rules that govern landing. Many previous studies have relied on tethered preparations to study landing behaviors, but tethering induces experimental artefacts by forcing some behaviors to operate in open-feedback control loop while others remain closed-loop. On the other hand, it is harder for the experimenter to control the stimuli experienced by freely-flying insects. One approach towards understanding general mechanisms of landing is to determine the common elements of their kinematics on surfaces of different orientations. We conducted a series of experiments in which the houseflies, Musca domestica, were lured to land on vertical (wall landings) or inverted (ceiling landings) substrates, while their flight was recorded with multiple high-speed cameras. We observed that, in both cases, well-controlled landings occurred when the distance at which flies initiated deceleration was proportional to flight velocity component in the direction of substrate. The ratio of substrate distance and velocity at onset of deceleration (tau) was conserved, despite substantial differences in mechanics of vertical vs. ceiling landings. When these conditions were not satisfied, their landing performance was compromised, causing their heads to collide into the substrate. Unlike body-deceleration, leg-extension in flies was independent of substrate distance or approach velocity. Thus, the robust reflexive visual initiation of deceleration is independent of substrate orientation, and combines with a more variable initiation of leg-extension which depends on surface orientation. Together, these combinations of behaviors enable flies to land in a versatile manner on substrates of various orientations.

}, issn = {1932-6203}, doi = {10.1371/journal.pone.0219861}, author = {Balebail, Sujay and Raja, Sathish K and Sane, Sanjay P} } @article {69323, title = {Tuneable reflexes control antennal positioning in flying hawkmoths.}, journal = {Nat Commun}, volume = {10}, year = {2019}, month = {2019 Dec 06}, pages = {5593}, abstract = {

Complex behaviours may be viewed as sequences of modular actions, each elicited by specific sensory cues in their characteristic timescales. From this perspective, we can construct models in which unitary behavioural modules are hierarchically placed in context of related actions. Here, we analyse antennal positioning reflex in hawkmoths as a tuneable behavioural unit. Mechanosensory feedback from two antennal structures, B{\"o}hm{\textquoteright}s bristles (BB) and Johnston{\textquoteright}s organs (JO), determines antennal position. At flight onset, antennae attain a specific position, which is maintained by feedback from BB. Simultaneously, JO senses deflections in flagellum-pedicel joint due to frontal airflow, to modulate its steady-state position. Restricting JO abolishes positional modulation but maintains stability against perturbations. Linear feedback models are sufficient to predict antennal dynamics at various set-points. We modelled antennal positioning as a hierarchical neural-circuit in which fast BB feedback maintains instantaneous set-point, but slow JO feedback modulates it, thereby elucidating mechanisms underlying its robustness and flexibility.

}, issn = {2041-1723}, doi = {10.1038/s41467-019-13595-3}, author = {Natesan, Dinesh and Saxena, Nitesh and Ekeberg, {\"O}rjan and Sane, Sanjay P} } @article {48893, title = {Fairyflies.}, journal = {Curr Biol}, volume = {28}, year = {2018}, month = {2018 Dec 03}, pages = {R1331-R1332}, abstract = {

A Quick Guide to fairyflies, miniature parasitoid wasps which have the smallest adult size known for any insect.

}, issn = {1879-0445}, doi = {10.1016/j.cub.2018.10.014}, author = {Palavalli-Nettimi, Ravindra and Sane, Sanjay P} } @article {24295, title = {Gene regulation and species-specific evolution of free-flight odor-tracking in Drosophila.}, journal = {Mol Biol Evol}, volume = {35}, year = {2018}, month = {01/2018}, pages = {3-15}, abstract = {

The flight ability of insects has coevolved with the development of organs necessary for takeoff from the ground, and to generate and modulate lift while flying in complex environments. Flight orientation to the appropriate food source and mating partner depends on the perception and integration of multiple chemical signals. We used a wind tunnel-based assay to investigate the natural and molecular evolution of free-flight odor-tracking behavior in Drosophila. First, the comparison of female and male flies of several populations and species revealed substantial sex-related, inter- and intra-specific variations for distinct flight features. In these flies, we compared the molecular structure of desat1, a fast-evolving gene involved in multiple aspects of pheromonal communication in Drosophila. We manipulated desat1 regulation and found that both neural and non-neural tissues influence distinct flight features. Together, our data suggest that desat1 is involved in the evolution of free-flight odor-tracking behaviors in Drosophila.

}, issn = {1537-1719}, doi = {10.1093/molbev/msx241}, author = {Houot, Benjamin and Cazal{\'e}-Debat, Laurie and Fraichard, St{\'e}phane and Everaerts, Claude and Saxena, Nitesh and Sane, Sanjay P and Ferveur, Jean-Fran{\c c}ois} } @article {36103, title = {The Mechanosensory-Motor Apparatus of Antennae in the Oleander hawk moth (Daphnis nerii, Lepidoptera).}, journal = {J Comp Neurol}, year = {2018}, month = {2018 Jun 15}, abstract = {

Insect antennae are sensory organs of great importance because they can sense diverse environmental stimuli. In addition to serving as primary olfactory organs of insects, antennae also sense a wide variety of mechanosensory stimuli, ranging from low-frequency airflow or gravity cues to high-frequency antennal vibrations due to sound, flight or touch. The basal segments of the antennae house multiple types of mechanosensory structures that prominently include the sensory hair plates, or B{\"o}hm{\textquoteright}s bristles, which measure the gross extent of antennal movement, and a ring of highly sensitive scolopidial neurons, collectively called the Johnston{\textquoteright}s organs, which record subtle flagellar vibrations. To fulfil their multifunctional mechanosensory role, the antennae of insects must actively move thereby enhancing their ability to sense various cues in the surrounding environment. This tight coupling between antennal mechanosensory function and antennal movements means that the underlying mechanosensory-motor apparatus constitutes a highly tuned feedback-controlled system. Our study aims to explore how the sensory and motor components of this system are configured to enable such functional versatility. We describe antennal mechanosensory neurons, their central projections in the brain relative to antennal motor neurons and the internal morphology of various antennal muscles that actuate the basal segments of the antenna. We studied these in the Oleander hawk moth (Daphnis nerii) using a combination of techniques such as neural dye fills, confocal microscopy, scanning electron microscopy and X-Ray tomography. Our study thus provides a detailed anatomical picture of the antennal mechanosensory-motor apparatus, which in turn provides key insights into its multifunctional role. This article is protected by copyright. All rights reserved.

}, issn = {1096-9861}, doi = {10.1002/cne.24477}, author = {Sant, Harshada H and Sane, Sanjay P} } @article {29628, title = {Odor source localization in complex visual environments by fruit flies.}, journal = {J Exp Biol}, volume = {221}, year = {2018}, month = {2018 Jan 19}, abstract = {

Flying insects routinely forage in complex and cluttered sensory environments. Their search for a food or a pheromone source typically begins with a whiff of odor, which triggers a flight response, eventually bringing the insect near the odor source. However, pinpointing the precise location of an odor source requires use of both visual and olfactory modalities, aided by odor plumes. Here, we investigated odor-tracking behavior in fruit flies (Drosophila melanogaster) presented with low- or high-contrast visual landmarks, either paired with or separate from an attractive odor cue. These experiments were conducted either in a gentle air stream which generated laminar odor plumes or in still air in which odor dissipates uniformly in all directions. Trajectories of flies revealed several novel features of their odor-tracking behavior in addition to those previously documented. First, in both moving and still air, odor-seeking flies rely on the co-occurrence of visual landmarks with olfactory cues to guide them to odorant objects. Second, flies abruptly decelerate upon encountering an odor plume, thereafter steering towards the nearest visual objects that had no inherent salience in the absence of odor. Thus, interception of an attractive odor increases their salience to nearby high-contrast visual landmarks. Third, flies adopt distinct odor-tracking strategies during flight in moving versus still air. Whereas they weave in and out of plumes towards an odor source in airflow, their approach is more incremental in still air. Both strategies are robust and flexible, and enable flies to reliably find odor sources under diverse visual and airflow environments.

}, issn = {1477-9145}, doi = {10.1242/jeb.172023}, author = {Saxena, Nitesh and Natesan, Dinesh and Sane, Sanjay P} } @article {48890, title = {The roles of vision and antennal mechanoreception in hawkmoth flight control.}, journal = {Elife}, volume = {7}, year = {2018}, month = {2018 12 10}, abstract = {

Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth They represent a large group of insects that use Johnston{\textquoteright}s organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.

}, issn = {2050-084X}, doi = {10.7554/eLife.37606}, author = {Dahake, Ajinkya and St{\"o}ckl, Anna L and Foster, James J and Sane, Sanjay P and Kelber, Almut} } @article {13640, title = {Eppur si vola (and yet it flies).}, journal = {J Exp Biol}, volume = {220}, year = {2017}, month = {2017 Feb 15}, pages = {514-516}, issn = {1477-9145}, doi = {10.1242/jeb.151324}, author = {Sane, Sanjay P} } @article {16561, title = {Mechanics of the thorax in flies.}, journal = {J Exp Biol}, volume = {220}, year = {2017}, month = {2017 Apr 15}, pages = {1382-1395}, abstract = {

Insects represent more than 60\% of all multicellular life forms, and are easily among the most diverse and abundant organisms on earth. They evolved functional wings and the ability to fly, which enabled them to occupy diverse niches. Insects of the hyper-diverse orders show extreme miniaturization of their body size. The reduced body size, however, imposes steep constraints on flight ability, as their wings must flap faster to generate sufficient forces to stay aloft. Here, we discuss the various physiological and biomechanical adaptations of the thorax in flies which enabled them to overcome the myriad constraints of small body size, while ensuring very precise control of their wing motion. One such adaptation is the evolution of specialized myogenic or asynchronous muscles that power the high-frequency wing motion, in combination with neurogenic or synchronous steering muscles that control higher-order wing kinematic patterns. Additionally, passive cuticular linkages within the thorax coordinate fast and yet precise bilateral wing movement, in combination with an actively controlled clutch and gear system that enables flexible flight patterns. Thus, the study of thoracic biomechanics, along with the underlying sensory-motor processing, is central in understanding how the insect body form is adapted for flight.

}, issn = {1477-9145}, doi = {10.1242/jeb.128363}, author = {Deora, Tanvi and Gundiah, Namrata and Sane, Sanjay P} } @article {5307, title = {Airflow and optic flow mediate antennal positioning in flying honeybees.}, journal = {Elife}, volume = {5}, year = {2016}, month = {2016}, abstract = {

To maintain their speeds during navigation, insects rely on feedback from their visual and mechanosensory modalities. Although optic flow plays an essential role in speed determination, it is less reliable under conditions of low light or sparse landmarks. Under such conditions, insects rely on feedback from antennal mechanosensors but it is not clear how these inputs combine to elicit flight-related antennal behaviours. We here show that antennal movements of the honeybee, Apis mellifera, are governed by combined visual and antennal mechanosensory inputs. Frontal airflow, as experienced during forward flight, causes antennae to actively move forward as a sigmoidal function of absolute airspeed values. However, corresponding front-to-back optic flow causes antennae to move backward, as a linear function of relative optic flow, opposite the airspeed response. When combined, these inputs maintain antennal position in a state of dynamic equilibrium.

}, issn = {2050-084X}, doi = {10.7554/eLife.14449}, author = {Roy Khurana, Taruni and Sane, Sanjay P} } @article {8758, title = {Neurobiology and biomechanics of flight in miniature insects.}, journal = {Curr Opin Neurobiol}, volume = {41}, year = {2016}, month = {2016 Oct 4}, pages = {158-166}, abstract = {

Miniature insects can be as small as a few hundred micrometres in size, making them among the smallest metazoan animals ever described. Yet, even at these length scales, they display remarkably sophisticated flight behaviours. For flight at such low Reynolds numbers, miniature insects have evolved biomechanical and neural adaptations that push the boundaries of what is possible in the realm of physics and neurobiology of flight. After several decades of relative dormancy, this question has recently been revisited by researchers working in diverse areas ranging from systematics and neurobiology to dispersal behaviours. In this review, I cover recent findings in this area, and point towards the many open questions that still remain unanswered.

}, issn = {1873-6882}, doi = {10.1016/j.conb.2016.09.008}, author = {Sane, Sanjay P} } @article {7039, title = {Orientation in high-flying migrant insects in relation to flows: mechanisms and strategies.}, journal = {Philos Trans R Soc Lond B Biol Sci}, volume = {371}, year = {2016}, month = {2016 Sep 26}, abstract = {

High-flying insect migrants have been shown to display sophisticated flight orientations that can, for example, maximize distance travelled by exploiting tailwinds, and reduce drift from seasonally optimal directions. Here, we provide a comprehensive overview of the theoretical and empirical evidence for the mechanisms underlying the selection and maintenance of the observed flight headings, and the detection of wind direction and speed, for insects flying hundreds of metres above the ground. Different mechanisms may be used-visual perception of the apparent ground movement or mechanosensory cues maintained by intrinsic features of the wind-depending on circumstances (e.g. day or night migrations). In addition to putative turbulence-induced velocity, acceleration and temperature cues, we present a new mathematical analysis which shows that {\textquoteright}jerks{\textquoteright} (the time-derivative of accelerations) can provide indicators of wind direction at altitude. The adaptive benefits of the different orientation strategies are briefly discussed, and we place these new findings for insects within a wider context by comparisons with the latest research on other flying and swimming organisms.This article is part of the themed issue {\textquoteright}Moving in a moving medium: new perspectives on flight{\textquoteright}.

}, issn = {1471-2970}, doi = {10.1098/rstb.2015.0392}, author = {Reynolds, Andy M and Reynolds, Don R and Sane, Sanjay P and Hu, Gao and Chapman, Jason W} } @article {861, title = {Biomechanical basis of wing and haltere coordination in flies.}, journal = {Proc Natl Acad Sci U S A}, volume = {112}, year = {2015}, month = {2015 Feb 3}, pages = {1481-6}, abstract = {

The spectacular success and diversification of insects rests critically on two major evolutionary adaptations. First, the evolution of flight, which enhanced the ability of insects to colonize novel ecological habitats, evade predators, or hunt prey; and second, the miniaturization of their body size, which profoundly influenced all aspects of their biology from development to behavior. However, miniaturization imposes steep demands on the flight system because smaller insects must flap their wings at higher frequencies to generate sufficient aerodynamic forces to stay aloft; it also poses challenges to the sensorimotor system because precise control of wing kinematics and body trajectories requires fast sensory feedback. These tradeoffs are best studied in Dipteran flies in which rapid mechanosensory feedback to wing motor system is provided by halteres, reduced hind wings that evolved into gyroscopic sensors. Halteres oscillate at the same frequency as and precisely antiphase to the wings; they detect body rotations during flight, thus providing feedback that is essential for controlling wing motion during aerial maneuvers. Although tight phase synchrony between halteres and wings is essential for providing proper timing cues, the mechanisms underlying this coordination are not well understood. Here, we identify specific mechanical linkages within the thorax that passively mediate both wing-wing and wing-haltere phase synchronization. We demonstrate that the wing hinge must possess a clutch system that enables flies to independently engage or disengage each wing from the mechanically linked thorax. In concert with a previously described gearbox located within the wing hinge, the clutch system enables independent control of each wing. These biomechanical features are essential for flight control in flies.

}, keywords = {Animals, Biomechanical Phenomena, Diptera, Microscopy, Electron, Scanning, Wings, Animal}, issn = {1091-6490}, doi = {10.1073/pnas.1412279112}, author = {Deora, Tanvi and Singh, Amit Kumar and Sane, Sanjay P} } @article {734, title = {Neural control of wing coordination in flies.}, journal = {Curr Biol}, volume = {25}, year = {2015}, month = {2015 Jan 5}, pages = {80-6}, abstract = {

At the onset of each flight bout in flies, neural circuits in the CNS must rapidly integrate multimodal sensory stimuli and synchronously engage hinges of the left and right wings for coordinated wing movements. Whereas anatomical and physiological investigations of flight have been conducted on larger flies, molecular genetic studies in Drosophila have helped identify neurons that mediate various levels of flight control. However, neurons that might mediate bilateral coordination of wing movements to precisely synchronize left and right wing engagement at flight onset and maintain their movement in perfect coordination at rapid frequencies during flight maneuvers remain largely unexplored. Wing coordination could be directly modulated via bilateral sensory inputs to motoneurons of steering muscles and/or through central interneurons. Using a Ca(2+)-activity-based GFP reporter, we identified three flight-activated central dopaminergic interneurons in the ventral ganglion, which connect to and activate motoneurons that innervate a pair of direct-steering flight muscles. The activation of these newly identified dopaminergic interneurons is context specific. Whereas bilateral wing engagement for flight requires these neurons, they do not control unilateral wing extension during courtship. Thus, independent central circuits function in the context of different natural behaviors to control the motor circuit for Drosophila wing movement.

}, keywords = {Animals, Central Nervous System, Dopaminergic Neurons, Drosophila, Flight, Animal, Genes, Reporter, Male, Synapses, Wings, Animal}, issn = {1879-0445}, doi = {10.1016/j.cub.2014.10.069}, author = {Sadaf, Sufia and Reddy, O Venkateswara and Sane, Sanjay P and Hasan, Gaiti} }