Hunting for the elusive “sixth” sense: navigation and magnetic sensation in a nocturnal migratory moth

Project Information

MagneticMoth

Grant agreement ID: 741298

DOI

10.3030/741298

Project closed

EC signature date 26 April 2017

Start date 1 September 2017

End date 31 August 2023

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 2 498 625,00

EU contribution

€ 2 498 625,00

Coordinated by

LUNDS UNIVERSITET
Sweden

Periodic Reporting for period 4 - MagneticMoth (Hunting for the elusive “sixth” sense: navigation and magnetic sensation in a nocturnal migratory moth)

Reporting period: 2022-03-01 to 2023-08-31

Summary of the context and overall objectives of the project

What is the problem/issue being addressed?

Many animals sense the Earth’s magnetic field and use it as a compass for long-distance navigation. However, an enduring mystery is how this magnetic field is sensed. No one has ever found the sensory organ or sensory cells responsible in any animal, and even though several plausible mechanisms explaining how the magnetic field might be sensed have been postulated, none have ever been proven. In this project, we aimed to solve this mystery in the comparatively simple nervous system of the Australian Bogong moth (Fig. 1), by studying it’s remarkable long-distance navigation. This moth makes a Spring migration of around 1000 km from its birthplace in an arid area of inland southeast Australia to a destination it is never previously visited (Fig. 1B) – cool alpine caves, high up in the Australian Alps (where it will spend the coming summer in a dormant state known as aestivation: Fig. 1C).

Why is it important for society?

Our desire to understand how animals sense and use the magnetic field is admittedly driven by sheer curiosity of how animals, even insects with tiny nervous systems, can solve such a difficult problem. Nonetheless, such robust long-distance navigational performance at night is immensely beneficial, not only for animals, but also for any kind of technological application that requires similar levels of performance. The robust high-performance solutions for control and guidance that have evolved in the animal kingdom over hundreds of millions of years hold clues for how similar systems can be implemented in technological applications.

What are the overall objectives?

A. To identify the principles underpinning the highly directed return migration of Bogong moths. We used state-of-the-art vertical radar and LIDAR methods to analyse the fine structure of Bogong moth swarms during their forward and return migrations to unravel the principles they use to maintain a precise migratory trajectory independent of the prevailing wind direction. Second, to understand the population dynamics of what is undoubtedly the most accurate and directed migration known in any nocturnal insect, we have used genetic methods to determine whether moths from different geographic origins aestivate in different alpine caves. Our aim was to obtain the most comprehensive picture ever obtained of migratory strategies in a nocturnal insect, and allow us to understand how a magnetic compass sense is used to hold a precise migratory course despite an unfavourable wind direction.

B. To determine how magnetic and visual cues are used for nocturnal navigation in migratory moths. We dissected how visual cues (terrestrial landmarks, the moon, stars) are used in combination with the Earth’s magnetic field to steer migration. Secondly, we attempted to determine which of the two current hypotheses for biological magnetoreception are used by the Bogong moth. Our aim was to obtain the first detailed description of how magnetic and visual cues are integrated to create a robust compass for long-distance navigation in insects.

C. To identify and physiologically characterise the peripheral receptor cells and central brain circuits responsible for the detection and analysis of the Earth’s magnetic field. We planned to target specific regions in the brain and nervous system with intracellular electrodes, with the aim of recording from, and physiologically characterising, candidate magnetoreceptive cells during magnetic stimulation. The aim was to discover the enigmatic magnetoreceptor, and to characterize the central brain circuits responsible for analysing magnetic information during long distance navigation. These would represent major advances, as neither is currently understood in any animal.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

A major task completed during the project – and which was (and will be) essential for our progress – was the construction of a new magnetic-free laboratory building at our field site in Australia (which is free from magnetic artefacts: Fig. 2). This is the only lab building of its kind in the southern hemisphere and only the second magnetic-free lab building in the world. This lab houses a non-magnetic electrophysiology rig (with Helmholtz coils to provide precise Earth-strength magnetic stimulation – Fig. 2C-D) and a behavioural arena (also with Helmholtz coils – Fig. 2F,G). We also replicated the non-magnetic electrophysiology lab in Lund.

The results of our project are as follows:

1. We have shown that nocturnal migratory insects - like nocturnal migratory birds - sense the Earth’s magnetic field and rely on it to determine compass directions (N, S, E and W) to steer migration in the inherited migratory direction (Fig. 3), which is a major discovery (and currently being repeated). We also investigated whether the Bogong moth magnetic sense is based on a light-dependent radical pair mechanism present in cryptochrome molecules. Unfortunately our attempts to localise where in the nervous system these cryptochromes reside (thus revealing the possible location of the magnetoreceptor) have so far been inconclusive. Moreover, the riskiest part of the project has also not succeeded so far (despite a large effort) – identification and characterisation of the elusive magnetic sensor and the higher-order cells in the brain that process magnetic information.

2. We have shown that the Bogong moth uses the Australian starry night sky as a true compass to steer migration in the inherited migratory direction (Fig. 4), the first invertebrate known to do so (the only other animals known to possess this ability are humans and some species of night-migratory birds). Moreover, the moths are able to compensate for the nightly rotations of the stars in order to maintain a constant migratory heading. These are also major discoveries. In addition, we have determined the structure of the Bogong moth brain [1] identified a number of visual cells in the moth’s central brain that respond exclusively to rotations of the starry night sky, and which are therefore likely to be involved in the stellar compass network that analyses stellar information to set and correct the migratory course (Fig. 5). This work is currently being written up for publication in Nature.

3. We have sequenced and annotated the genome of the Bogong moth. This is allowing us (and others) to ask a number of very important fundamental questions regarding the biology, ecology, conservation, migration and sensory biology of this keystone species (whose mass migration to the Australian Alps is critically important for the health of the alpine ecosystem). This work is currently being written up for publication in iScience.

4. We used the new genome to show that the Bogong moth population has no genetic structure (i.e. it is panmictic: [2]). Nonetheless we were able to show that there are four genetic loci tightly coupled to the geographic origin of the moths, and thus to the inherited migratory direction, suggesting that the migratory direction is indeed passed down from generation to generation at each geographical location within the vast breeding grounds of the Bogong moth.

5. We have pioneered new methods for detecting and tracking migrating insects [2-7]. Our new automatic camera tracking system (“Camfi”) and our new vertical LIDAR system (Fig. 6), coupled with traditional vertical radar, will allow us and others to identify, monitor and track insects during their migration with unprecedented clarity. These methods are currently being used in the field to monitor populations of the endangered Bogong moth, and can be used for monitoring the health of insect populations in regions of the world where their decline is extremely worrying.

[1] Adden, A., Wibrand, S., Pfeiffer, K., Warrant, E.J. and Heinze, S. (2020). The brain of a nocturnal migratory insect, the Australian Bogong moth. Journal of Comparative Neurology 528: 1942-1963. doi: 10.1002/cne.24866.

[2] Wallace, J.R.A Maleszka, R. and Warrant, E.J. (2023). Large-scale whole-genome sequencing of migratory Bogong moths Agrotis infusa reveals genetic variants associated with migratory direction in a panmictic population. Manuscript. bioRxiv 2022.05.27.49380 doi.org/10.1101/2022.05.27.493801

[3] Hao, Z., Drake, V.A. Taylor, J.R. and Warrant, E.J. (2020). Insect target classes discerned from entomological radar data. Remote Sensing 2: 673. doi:10.3390/rs12040673.

[4] Drake, V.A. Hao, Z. and Warrant, E.J. (2021). Heading variations resolve the heading-direction ambiguity in vertical-beam radar observations of insect migration. International Journal of Remote Sensing 42: 3873-3898. https://doi.org/10.1080/01431161.2021.1883202

[5] Li, M., Seinsche, C., Jansson, S., Hernandez, J., Rota, J., Warrant, E.J. and Brydegaard, M. (2022). Potential for identification of wild night-flying moths by remote infrared microscopy. Journal of the Royal Society Interface 19: 20220256. doi.org/10.1098/rsif.2022.0256

[6] Wallace, J.R.A Reber, T., Dreyer, D., Beaton, B., Zeil, J. and Warrant, E.J. (2023). Camera-based automated monitoring of flying insects (Camfi). I. Field and computational methods. Frontiers in Insect Science 3:1240400. doi.org/10.3389/finsc.2023.1240400.

[7] Wallace, J.R.A Dreyer, D., Reber, T., Khaldy, L., Mathews-Hunter, B., Green, K., Zeil, J. and Warrant, E.J. (2023). Camera-based automated monitoring of flying insects in the wild (Camfi). II. Flight behaviour and long-term population monitoring of migratory Bogong moths in Alpine Australia. Frontiers in Insect Science 3:1230501. doi.org/10.3389/finsc.2023.1230501

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

We progressed well beyond the state-of-the-art in several areas. Our finding of a magnetic sense in the Bogong moth, and the ability of this moth to use the Earth’s magnetic field as a true compass to migrate along its inherited migratory direction, are major discoveries. Equally major is the discovery of a parallel stellar compass (and underlying brain circuitry), making the Bogong moth the first invertebrate with a capacity to use the stars for navigation, alongside only humans and some species of night-migratory songbirds. Our most recent finding of an odour compound emitted from each alpine cave acting as a final navigational cue at the end of the moth’s long migratory journey, is also an unexpected and major discovery. Finally, our finding of four genetic loci tightly coupled to the inherited migratory direction, even though we currently don’t yet understand the meaning of these loci for migration, is also a very important discovery.

These discoveries show that natural sensory cues - in this case visual, olfactory and magnetic cues - are used to solve a complex navigational problem in an animal whose brain occupies a volume a fraction that of a grain of rice. This impressive ability adds significant new evidence supporting the idea that the insect nervous system, despite its small size, is both sophisticated and remarkable.

Fig. 1. The Australian Bogong moth Agrotis infusa

Fig.6. The new entomological LIDAR

Fig. 5. Brain cells responding to rotations of the starry night sky

Fig. 3. A magnetic compass in Bogong moths

Fig. 2. The ferromagnetic-free laboratory in Australia

Fig. 4. A stellar compass in Bogong moths