The brain behind straight-line orientation in dung beetles

Jundi, Basil el; Baird, Emily; Byrne, Marcus J.; Dacke, Marie

doi:10.1242/jeb.192450

Cited by 46 publications

(43 citation statements)

References 102 publications

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“…As in all insects, the Bogong moth CX is characterized by horizontal layers and vertical slices, which are most visible in the EB. This arrangement is identical to that in the locust (Williams, ) and the dung beetle (el Jundi, Baird, Byrne, & Dacke, ). Across many insects, the columnar structure results from a highly conserved underlying neural organization (el Jundi et al, ; Heinze, Florman, Asokaraj, el Jundi, & Reppert, ; Heinze & Homberg, ; Wolff, Iyer, & Rubin, ).…”

Section: Discussionsupporting

confidence: 65%

The brain of a nocturnal migratory insect, the Australian Bogong moth

Adden

Wibrand

Pfeiffer

et al. 2020

J of Comparative Neurology

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Every year, millions of Australian Bogong moths (Agrotis infusa) complete an astonishing journey: In Spring, they migrate over 1,000 km from their breeding grounds to the alpine regions of the Snowy Mountains, where they endure the hot summer in the cool climate of alpine caves. In autumn, the moths return to their breeding grounds, where they mate, lay eggs and die. These moths can use visual cues in combination with the geomagnetic field to guide their flight, but how these cues are processed and integrated into the brain to drive migratory behavior is unknown. To generate an access point for functional studies, we provide a detailed description of the Bogong moth's brain.Based on immunohistochemical stainings against synapsin and serotonin (5HT), we describe the overall layout as well as the fine structure of all major neuropils, including the regions that have previously been implicated in compass-based navigation. The resulting average brain atlas consists of 3D reconstructions of 25 separate neuropils, comprising the most detailed account of a moth brain to date. Our results show that the Bogong moth brain follows the typical lepidopteran ground pattern, with no major specializations that can be attributed to their spectacular migratory lifestyle. These findings suggest that migratory behavior does not require widespread modifications of brain structure, but might be achievable via small adjustments of neural circuitry in key brain areas. Locating these subtle changes will be a challenging task for the future, for which our study provides an essential anatomical framework. K E Y W O R D S central complex, insect brain, Lepidoptera, mushroom body, noctuid 1 | INTRODUCTION One of the central questions in neuroscience is how animal behaviors result from neural computations. From the sensory input that elicits abehavior to the motor circuits that execute it-the neural processing is complex and, as yet, we only understand small pieces of this multi-level puzzle. To delve deeper into this question, we need an animal model that shows a robust behavior and whose brain is accessible enough to

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Section: Discussionsupporting

confidence: 65%

The brain of a nocturnal migratory insect, the Australian Bogong moth

Adden

Wibrand

Pfeiffer

et al. 2020

J of Comparative Neurology

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“…Insects are able to combine these multiscale, multireference, and multimodal compasses in different, flexible manners depending on the context or particular ecology. For example, dung beetles trying to maintain a straight course away from the crowded dung pile, simply minimise any change in sensory input across their short journey (el Jundi et al 2016(el Jundi et al , 2019Dacke et al 2019), whereas central place foragers that visit the same feeding site over successive days, or migratory insects that navigate for long periods per day, use matched filters (Wehner 1987a(Wehner , 1989Bech et al 2014;Warrant 2016) to derive a robust, time-invariant, geocentric compass. Desert ants and dung beetles demonstrate the flexible transfer of orientation information from one modality to another (wind to celestial: Dacke et al 2019); visual to celestial (Schwarz et al 2017a); between polarisation and sun compass (Lebhardt and Ronacher 2015)) to markedly extend their behavioural capacity.…”

Section: Multimodality Within the Insect Compass Systemmentioning

confidence: 99%

Multimodal interactions in insect navigation

2020

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Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species' sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities.Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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“…As in all insects, the Bogong moth CX consists of the fan-shaped body (FB, or CBU), the ellipsoid body (EB, or CBL), the protocerebral bridge (PB) and the noduli (NO). The EB is visibly divided into 9 lateral columns, identically to the locust (Williams, 1975) and the dung beetle (el Jundi, Baird, Byrne, & Dacke, 2019). In the butterfly, locust, fruit fly and beetle, this columnar structure has been shown to result from a highly conserved underlying neural organisation (el Jundi et al, 2019;Heinze, Florman, Asokaraj, el Jundi, & Reppert, 2013;Heinze & Homberg, 2008;Wolff, Iyer, & Rubin, 2015).…”

Section: Central and Lateral Complexmentioning

confidence: 99%

“…The EB is visibly divided into 9 lateral columns, identically to the locust (Williams, 1975) and the dung beetle (el Jundi, Baird, Byrne, & Dacke, 2019). In the butterfly, locust, fruit fly and beetle, this columnar structure has been shown to result from a highly conserved underlying neural organisation (el Jundi et al, 2019;Heinze, Florman, Asokaraj, el Jundi, & Reppert, 2013;Heinze & Homberg, 2008;Wolff, Iyer, & Rubin, 2015). These columnar neurons form the basis of a neural circuit that uses both external and internal sensory cues to encode heading direction Turner-Evans et al, 2017).…”

Section: Central and Lateral Complexmentioning

confidence: 99%

The brain of a nocturnal migratory insect, the Australian Bogong moth

Adden

Wibrand

Pfeiffer

et al. 2019

Preprint

View full text Add to dashboard Cite

Every year, millions of Australian Bogong moths (Agrotis infusa) complete an astonishing journey: in spring, they migrate from their breeding grounds to the alpine regions of the Snowy Mountains, where they endure the hot summer in the cool climate of alpine caves. In autumn, the moths return to their breeding grounds, where they mate, lay eggs and die. Each journey can be over 1000 km long and each moth generation completes the entire roundtrip. Without being able to learn any aspect of this journey from experienced individuals, these moths can use visual cues in combination with the geomagnetic field to guide their flight. How these cues are processed and integrated in the brain to drive migratory behaviour is as yet unknown. Equally unanswered is the question of how these insects identify their targets, i.e. specific alpine caves used as aestivation sites over many generations. To generate an access point for functional studies aiming at understanding the neural basis of these insect's nocturnal migrations, we provide a detailed description of the Bogong moth's brain. Based on immunohistochemical stainings against synapsin and serotonin (5HT), we describe the overall layout as well as the fine structure of all major neuropils, including all regions that have previously been implicated in compass-based navigation. The resulting average brain atlas consists of 3D reconstructions of 25 separate neuropils, comprising the most detailed account of a moth brain to date. Our results show that the Bogong moth brain follows the typical lepidopteran ground pattern, with no major specializations that can be attributed to their spectacular migratory lifestyle. Comparison to the brain of the migratory Monarch butterfly revealed nocturnal versus diurnal lifestyle and phylogenetic identity as the dominant parameters determining large-scale neuroarchitecture. These findings suggest that migratory behaviour does not require widespread modifications of brain structure, but might be achievable via small adjustments of neural circuitry in key brain areas. Locating these subtle changes will be a challenging task for the future, for which our study provides an essential anatomical framework.

show abstract

The brain behind straight-line orientation in dung beetles

Cited by 46 publications

References 102 publications

The brain of a nocturnal migratory insect, the Australian Bogong moth

The brain of a nocturnal migratory insect, the Australian Bogong moth

Multimodal interactions in insect navigation

The brain of a nocturnal migratory insect, the Australian Bogong moth

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