Neural coding underlying the cue preference for celestial orientation

Diurnal and nocturnal African dung beetles use celestial cues, such as the sun, the moon, and the polarization pattern, to roll dung balls along straight paths across the savanna. Although nocturnal beetles move in the same manner through the same environment as their diurnal relatives, they do so when light conditions are at least 1 million-fold dimmer. Here, we show, for the first time to our knowledge, that the celestial cue preference differs between nocturnal and diurnal beetles in a manner that reflects their contrasting visual ecologies. We also demonstrate how these cue preferences are reflected in the activity of compass neurons in the brain. At night, polarized skylight is the dominant orientation cue for nocturnal beetles. However, if we coerce them to roll during the day, they instead use a celestial body (the sun) as their primary orientation cue. Diurnal beetles, however, persist in using a celestial body for their compass, day or night. Compass neurons in the central complex of diurnal beetles are tuned only to the sun, whereas the same neurons in the nocturnal species switch exclusively to polarized light at lunar light intensities. Thus, these neurons encode the preferences for particular celestial cues and alter their weighting according to ambient light conditions. This flexible encoding of celestial cue preferences relative to the prevailing visual scenery provides a simple, yet effective, mechanism for enabling visual orientation at any light intensity.The blue sky is a rich source of visual cues that are used by many animals during orientation or navigation (1, 2). Besides the sun, celestial phenomena, such as the skylight intensity gradient or the more complex polarization pattern, can serve as references for spatial orientation (3–5). Polarized skylight is generated by scattered sunlight in the atmosphere, and to a terrestrial observer, the resulting alignment of the electric field vectors extends across the entire sky, forming concentric circles around the position of the sun (Fig. 1A). A similar distribution of brightness and polarization pattern is also created around the moon (6). Although this nocturnal pattern is 1 million-fold dimmer than the daylight pattern (6), some animals, such as South African ball-rolling dung beetles, can use this lunar polarization pattern for orientation (7). To avoid competition for food at the dung pile, these beetles detach a piece of dung, shape it into a ball, and roll it away along a straight-line path. For this type of straight-line orientation, nocturnal beetles seem to rely exclusively on celestial cues (8), such as the moon or polarized light.Open in a separate windowFig. 1.Celestial cue preference in dung beetles under a natural sky. (A) Schematic illustration of the polarization pattern around a celestial body (sun or moon). Change of direction in diurnal (D, Left) and nocturnal (N, Right) beetles rolling under a sun-lit (B) or moon-lit (C) sky. The change of direction was calculated as the angular difference between two consecutive rolls, either without manipulation (control, ●) or when the sun or moon was reflected to the opposite sky hemisphere between the two rolls (test, ○). The mean directions (μ) are indicated by black (control) or red (test) lines, and error bars indicate circular SDs. (B) Without manipulation, both species kept the direction [P < 0.001 by V test; μ_diurnal (±SD) = 2.6° ± 17.98°, n = 20; μ_nocturnal = −8.7° ± 38.34°, n = 20). When the sun was reflected to the opposite sky hemisphere (and the real sun was shaded), both species responded to this change (P < 0.001 by V-test; μ_diurnal = 178.9° ± 54.6°, n = 20; μ_nocturnal = 163.8° ± 46.58°, n = 20). (C) Under the moon in the control experiments, both species showed a constant rolling direction (P < 0.001 by V test; μ_diurnal = 3.1° ± 35.39°, n = 20; μ_nocturnal = −3.3° ± 37.87°, n = 20). When the moon was reflected to the opposite sky hemisphere, the diurnal species followed the position change of the moon (P = 0.002 by V test; μ = 179.5° ± 72.37°, n = 20), whereas the nocturnal species continued rolling in the original rolling direction (P < 0.001 by V test; μ = −13.4° ± 74.27°, n = 20).As with all nocturnal animals, night-active beetles have to overcome a major challenge: They need to maintain high orientation precision even under extremely dim light conditions. Indeed, recent experiments have shown that nocturnal dung beetles orient at night with the same precision as their diurnal relatives during the day (9), an ability partly due to the fact that their eyes are considerably more sensitive than the eyes of species that are active at brighter light levels (10–12). Nonetheless, for each species, orientation precision relies on being tuned to the most reliable celestial compass cue that is available during the animal’s normal activity window. How salient are these cues for nocturnal and diurnal species? Do diurnal species have a different celestial cue preference than nocturnal species? If so, how are these preferences represented neurally in the brain?In this study, we present a detailed picture of how the orientation systems of two closely related nocturnal and diurnal animals have been adapted to the ambient light conditions, combining behavioral experiments from the field with electrophysiological investigations of the underlying neural networks. Using behavioral experiments, we show that nocturnal dung beetles switch from a compass that uses a discrete celestial body (the sun) during the day to a celestial polarization compass for dim light orientation at night, whereas diurnal beetles use a celestial body (the sun or moon) for orientation at all light levels. In a second step, we simulated these skylight cues (the sun or moon and the polarization pattern) while electrophysiologically recording responses from neurons in the dung beetle’s central complex, a brain area that has been suggested to house the internal compass for celestial orientation (13, 14). These neural data precisely matched the cue preferences observed in behavioral field trials and show how an animal’s visual ecology influences the neural activity of its sky compass neurons. Our results also reveal, for the first time to our knowledge, how a weighting of celestial orientation cues could be neurally encoded in an animal brain.