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ABSTRACT Aggregation in social fishes has evolved to improve safety from predators. The individual interaction mechanisms that govern collective behavior are determined by the sensory systems that translate environmental information into behavior. In dynamic environments, shifts in conditions impede effective visual sensory perception in fish schools, and may induce changes in the collective response. Here, we consider whether environmental conditions that affect visual contrast modulate the collective response of schools to looming predators. By using a virtual environment to simulate four contrast levels, we tested whether the collective state of minnow fish schools was modified in response to a looming optical stimulus. Our results indicate that fish swam slower and were less polarized in lower contrast conditions. Additionally, schooling metrics known to be regulated by non-visual sensory systems tended to correlate better when contrast decreased. Over the course of the escape response, schools remained tightly formed and retained the capability of transferring social information. We propose that when visual perception is compromised, the interaction rules governing collective behavior are likely to be modified to prioritize ancillary sensory information crucial to maximizing chance of escape. Our results imply that multiple sensory systems can integrate to control collective behavior in environments with unreliable visual information.more » « less
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Abstract With a great variety of shapes and sizes, compound eye morphologies give insight into visual ecology, development, and evolution, and inspire novel engineering. In contrast to our own camera-type eyes, compound eyes reveal their resolution, sensitivity, and field of view externally, provided they have spherical curvature and orthogonal ommatidia. Non-spherical compound eyes with skewed ommatidia require measuring internal structures, such as with MicroCT (µCT). Thus far, there is no efficient tool to characterize compound eye optics, from either 2D or 3D data, automatically. Here we present two open-source programs: (1) the ommatidia detecting algorithm (ODA), which measures ommatidia count and diameter in 2D images, and (2) a µCT pipeline (ODA-3D), which calculates anatomical acuity, sensitivity, and field of view across the eye by applying the ODA to 3D data. We validate these algorithms on images, images of replicas, and µCT eye scans from ants, fruit flies, moths, and a bee.more » « less
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Abstract Explanations of why nocturnal insects fly erratically around fires and lamps have included theories of “lunar navigation” and “escape to the light”. However, without three-dimensional flight data to test them rigorously, the cause for this odd behaviour has remained unsolved. We employed high-resolution motion capture in the laboratory and stereo-videography in the field to reconstruct the 3D kinematics of insect flights around artificial lights. Contrary to the expectation of attraction, insects do not steer directly toward the light. Instead, insects turn their dorsum toward the light, generating flight bouts perpendicular to the source. Under natural sky light, tilting the dorsum towards the brightest visual hemisphere helps maintain proper flight attitude and control. Near artificial sources, however, this highly conserved dorsal-light-response can produce continuous steering around the light and trap an insect. Our guidance model demonstrates that this dorsal tilting is sufficient to create the seemingly erratic flight paths of insects near lights and is the most plausible model for why flying insects gather at artificial lights.more » « less
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Temporal ecological niche partitioning is an underappreciated driver of speciation. While insects have long been models for circadian biology, the genes and circuits that allow adaptive changes in diel-niches remain poorly understood. We compared gene expression in closely related day- and night-active non-model wild silk moths, with otherwise similar ecologies. Using an ortholog-based pipeline to compare RNA-Seq patterns across two moth species, we find over 25 pairs of gene orthologs showing differential expression. Notably, the genedisco,involved in circadian control, optic lobe and clock neuron development inDrosophila, shows robust adult circadian mRNA cycling in moth heads.Discois highly conserved in moths and has additional zinc-finger domains with specific nocturnal and diurnal mutations. We proposediscoas a candidate gene for the diversification of temporal diel-niche in moths.more » « less
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Abstract BackgroundInsects have evolved complex visual systems and display an astonishing range of adaptations for diverse ecological niches. Species ofDrosophila melanogastersubgroup exhibit extensive intra- and interspecific differences in compound eye size. These differences provide an excellent opportunity to better understand variation in insect eye structure and the impact on vision. Here we further explored the difference in eye size betweenD. mauritianaand its sibling speciesD. simulans. ResultsWe confirmed thatD. mauritianahave rapidly evolved larger eyes as a result of more and wider ommatidia thanD. simulanssince they recently diverged approximately 240,000 years ago. The functional impact of eye size, and specifically ommatidia size, is often only estimated based on the rigid surface morphology of the compound eye. Therefore, we used 3D synchrotron radiation tomography to measure optical parameters in 3D, predict optical capacity, and compare the modelled vision to in vivo optomotor responses. Our optical models predicted higher contrast sensitivity forD. mauritiana, which we verified by presenting sinusoidal gratings to tethered flies in a flight arena. Similarly, we confirmed the higher spatial acuity predicted forDrosophila simulanswith smaller ommatidia and found evidence for higher temporal resolution. ConclusionsOur study demonstrates that even subtle differences in ommatidia size between closely relatedDrosophilaspecies can impact the vision of these insects. Therefore, further comparative studies of intra- and interspecific variation in eye morphology and the consequences for vision among otherDrosophilaspecies, other dipterans and other insects are needed to better understand compound eye structure–function and how the diversification of eye size, shape, and function has helped insects to adapt to the vast range of ecological niches.more » « less
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Haematophagous mosquitoes need a blood meal to complete their reproductive cycle. To accomplish this, female mosquitoes seek vertebrate hosts, land on them and bite. As their eggs mature, they shift attention away from hosts and towards finding sites to lay eggs. We asked whether females were more tuned to visual cues when a host-related signal, carbon dioxide, was present, and further examined the effect of a blood meal, which shifts behaviour to ovipositing. Using a custom, tethered-flight arena that records wing stroke changes while displaying visual cues, we found the presence of carbon dioxide enhances visual attention towards discrete stimuli and improves contrast sensitivity for host-seeking Aedes aegypti mosquitoes. Conversely, intake of a blood meal reverses vertical bar tracking, a stimulus that non-fed females readily follow. This switch in behaviour suggests that having a blood meal modulates visual attention in mosquitoes, a phenomenon that has been described before in olfaction but not in visually driven behaviours.more » « less
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null (Ed.)Stabilizing responses to sideslip disturbances are a critical part of the flight control system in flies. While strongly mediated by mechanoreception, much of the final response results from the wide-field motion detection system associated with vision. In order to be effective, these responses must match the disturbance they are aimed to correct. To do this, flies must estimate the velocity of the disturbance, although it is not known how they accomplish this task when presented with natural images or dot fields. The recent finding, that motion parallax in dot fields can modulate stabilizing responses only if perceived below the fly, raises the question of whether other image statistics are also processed differently between eye regions. One such parameter is the density of elements moving in translational optic flow. Depending on the habitat, there might be strong differences in the density of elements providing information about self-motion above and below the fly, which in turn could act as selective pressures tuning the visual system to process this parameter on a regional basis. By presenting laterally moving dot fields of different densities we found that, in Drosophila melanogaster , the amplitude of the stabilizing response is significantly affected by the number of elements in the field of view. Flies countersteer strongly within a relatively low and narrow range of element densities. But this effect is exclusive to the ventral region of the eye, and dorsal stimuli elicit an unaltered and stereotypical response regardless of the density of elements in the flow. This highlights local specialization of the eye and suggests the lower region may play a more critical role in translational flight stabilization.more » « less
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null (Ed.)Flies and other insects use incoherent motion (parallax) to the front and sides to measure distances and identify obstacles during translation. Although additional depth information could be drawn from below, there is no experimental proof that they use it. The finding that blowflies encode motion disparities in their ventral visual fields suggests this may be an important region for depth information. We used a virtual flight arena to measure fruit fly responses to optic flow. The stimuli appeared below ( n = 51) or above the fly ( n = 44), at different speeds, with or without parallax cues. Dorsal parallax does not affect responses, and similar motion disparities in rotation have no effect anywhere in the visual field. But responses to strong ventral sideslip (206° s −1 ) change drastically depending on the presence or absence of parallax. Ventral parallax could help resolve ambiguities in cluttered motion fields, and enhance corrective responses to nearby objects.more » « less
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