The neural basis of nocturnal migration – generating an average-shape brain of the Bogong moth

Abstract

The long-distance migration that some animals accomplish can be truly astonishing. It can be observed in several different groups of animals with some of the most famous examples being sea turtles, birds, salmon and the Monarch butterfly. How these animals manage to navigate over distances sometimes as long as 10000 km nobody knows for sure. There is evidence of some animal’s ability to navigate using a so-called inner compass that is facilitated by the Earth’s magnetic field. The Earth’s magnetic field differs globally in strength and inclination angle, which can be used as a reference of direction. This ability is most feasible in animals whose lifestyle includes navigating in environments with a limited source of visual cues. One example of such an animal is the Bogong moth (Agrotis infusa). Each spring, it sets out on a journey up to a 1000 km long, reaching from their breeding grounds in northern NSW Australia towards the Australian Alps where they aestivate. This aestivation is not unlike hibernation and lasts for a few months. What follows, is a long journey back where they mate, lay eggs and die. How they are able to do this, with a brain the size of a grain of rice is yet unknown, but preliminary experiments points to an ability to navigate using the Earth’s magnetic field. This combination of a simple nervous system and a complex migratory behavior makes the Bogong moth an ideal model for understanding the neural basis of nocturnal migration. To further understand the function of a nervous system, it is important to also investigate its structure, since the function and structure of a nervous system are tightly linked. In this study, we created a standardized 3D average-shape Bogong moth brain based on anti-synapsin stained whole-mount preparations from ten individuals. This atlas provides a spatial frame of reference for comparisons between and within species and allows embedding neuronal data from studies examining the ability of the Bogong moth to use the magnetic field. With the aim of increasing our understanding of the neural basis of nocturnal navigation, we also reconstructed the brain of the Bogong moth’s non-migratory equivalent, the Turnip moth (Agrotis segetum) and used previously made reconstructions of the night-active Bogong moth’s day-active equivalent, the migratory Monarch butterfly Danaus plexippus to do volumetric comparisons between the different species neuropils. We also reconstructed one female Bogong brain to look for potential sexual dimorphism. Previous studies have shown that the ecology and lifestyle of an animal can be reflected in its brain anatomy, something that is supported by our results concerning differences in brain anatomy in day-active and night-active animals. However, according to our results there is no easy way to tell by brain structure if a species is migratory or not, and one must look further than on just neuropil level. Here, we present the most detailed insect brain ever reconstructed. Our standardized 3D average-shape Bogong moth brain will facilitate linking function to structure and will be an important component when further investigating the neural basis of nocturnal navigation.

Popular Abstract

Nocturnal long-distance migrants - making their way in darkness with a brain the size of grain of rice

Each spring, the Australian Bogong moth (Agrotis infusa) sets of on an astonishing journey. Their journey will be over a 1000 km long reaching from their breeding grounds to the Australian Alps where they seek shelter in isolated cool high-ridge top caves. Once in these caves they enter a dormant state for a few months, and at the onset of autumn they begin their long journey back. This may remind you of another more famous migratory insect, the Monarch butterfly. However, unlike the Monarch butterfly, the Bogong moth is a night-active species and therefore rely on nocturnal navigational cues when orienting and navigating.
Many night-active insects have sufficient visual sensitivity to distinguish nocturnal visual cues and to exploit them when orienting and navigating. Examples of cues that could be used during the night are the stars, the moon, the bright stripe of the Milky Way and the Earth’s magnetic field. What the Bogong moth uses is yet to be discovered. However, in a previous study, a nocturnal moth species (Noctua pronuba) was able to orient in a fixed direction without any visual cues, suggesting that an exclusive reliance on e.g. a lunar or a polarization compass can be ruled out for this moth species and that the possibility of exploitation of the Earth’s magnetic field should be considered. These data are strongly supported by preliminary experiments on the Bogong moth.

Previous studies have shown that the ecology and lifestyle of insects often is reflected in their brain anatomy. For example do insects that heavily rely on olfactory cues have a tendency to invest a greater fraction of neural tissue into olfaction processing. The insect brain is just like our brain, divided into different areas, where each area has its own function. In the insect brain, these are called neuropils. These neuropils can be grouped according to function, i.e. compass, optic, olfactory and learning/memory neuropils.

The combination of a simple nervous system and a complex migratory behaviour makes the Bogong moth an ideal model for understanding the neural basis of nocturnal navigation. In my project, I have created a 3-dimensional standardized average-shape brain of the male Bogong moth. It is based on the brain anatomy from ten individuals.

To come one step closer in unravelling the secrets behind nocturnal navigation, we compared the Bogong brain to the brain of its non-migratory equivalent, the Turnip moth (Agrotis segetum). This comparison was done by reconstructing a Turnip moth brain and extracting its neuropil volumes. By comparing these closely related migratory and non-migratory moth species, one could potentially find which neuropils demand more investment when being a long-distance migrant. To further investigate what the neural basis of long-distance migration looks like, it is important to examine the brains of both day-active and night-active migrants. Hence, we compared the brain of a Bogong moth to the brain of a Monarch butterfly, to potentially find the common aspects of brain morphology that could be linked to migration and that are independent of lifestyle. This comparison was done using volumetric data from previous studies on the monarch butterfly. We did, however not find any proof of a migratory behaviour being reflected in brain morphology. We did however find brain morphology differenes that could be linked to more innate behaviours. Our Bogong brain atlas provides a common spatial frame of reference that allows embedding neuronal data from studies examining the ability of the Bogong moth to use the magnetic field. Further, by using this standardized brain model of the Bogong moth as a 3D reference atlas combining neuronal data from many individuals, our results will facilitate interpretation of functional data obtained from behavioural and electrophysiological experiments.

Advisor: Stanley Heinze
Master’s Degree Project in Biology 45 credits 2016.
Department of Biology, Lund University

• author: Christensson, Sara
• supervisor: Stanley Heinze
• organization: Degree Projects in Biology
• course: BION01 20161
• year: 2016
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 8891293
• date added to LUP: 2016-09-09 12:09:13
• date last changed: 2016-09-09 12:09:13