Ancient Greek philosopher and scientist Aristotle classified over 500 species of birds, mammals and fish. Finely in tune with the natural world, his analyses deciphered many of the processes that occur in nature for the first time and endured for centuries. However, from time to time some of his observations were a little removed from reality. Every year, as summer drew to a close and winter set in, Aristotle saw something that he couldn’t explain. He noticed a dramatic shift in the animal species surrounding him. Of particular interest was the complete disappearance of the orange-tailed Redstart and its replacement by the orange-breasted Robin. Aristotle believed that what he was observing was a ‘transmutation’ of one bird-species into another as the seasons changed. After all, how else could anyone explain never seeing the birds together? Of course, Aristotle hadn’t discovered a unique shape-shifting bird species; he was in fact observing one of the many seasonal migrations that relentlessly carry animals around the planet.
In the millennia since Aristotle’s discovery of ‘transmutation’ we have come to know a great deal of the where, the why and the how of animal migration. Throughout the year, animal species travel vast distances in search of warmer climes, breeding grounds or in search of food, and often all three. One species whose migration has proved a tough nut to crack is one of the smallest of all migratory species: the Monarch Butterfly.While some migrations are clear for all to see, certain migratory species are only just revealing their secrets. As I type this, the Monarch butterfly is gradually spreading northwards through the North-Eastern United States and Southern Canada. As far as their migration is concerned, this is the end of their story, begun generations ago in the fall. As the days grow shorter and the mercury drops the Monarchs begin their journey. They flutter southwards through the American Midwest, before dropping further, out of the United States altogether, the burgeoning Rockies on one flank and the Gulf of Mexico on the other. Finally, just as winter begins to fully set in, they settle at their winter breeding grounds in the Fir groves of Central Mexico. For an insect with a relatively undeveloped immune system and a short lifespan, this is a leviathan journey (to see their journey in full, enlarge the image on the left). In total, they will have travelled 4000 km and astonishingly each population will settle within 1 km of the last. This journey is so immense that if we decided to set out on one of the same scale, we would eventually circumnavigate the planet with enough mileage left in the bank to go more than half way round again.
After the overwintering period is over, the butterflies, including females freshly laden with eggs, will return to their thawing homes. In perfect synchronicity with the germinating milkweed in the States, the obligate larval food source, the females lay their eggs and their offspring will carry on the final straight. As spring returns, the Monarchs disperse throughout the Pacific North East and the story is completed. In the fall, this generation will begin the cycle again.
As the details of the Monarchs’ leviathan journey became clear, it became obvious that they had a secret weapon their arsenal. The Monarch migration is almost unique in the natural world, with each migrating population undertaking its maiden voyage. This implies that the Monarchs have a hard-wired, genetic tool that guides them their destination; the route is not imprinted on them by previous generations.
There are crucial tools for any journey. If you were to find yourself abandoned in the middle of nowhere, you would hypothetically only need two things: a map (you have to know where your destination is relative to where you begin) and a compass (you have to know where you are going). The latter was the first system to truly be unravelled in Monarchs.
Just as humans have been doing for millennia, it has become clear that Monarchs use the Sun to orientate themselves. After all, the Sun always rises in the East and sets in the West — a handy piece of information
to know when orientating yourself. The problem with orientating oneself by following the Sun is that while your destination may be a fixed point, the position of the Sun is not. If their solar orientation was based only on following the position of the Sun, Monarchs would most definitely be dragged away from their south westerly heading as the Sun made its way across the sky. Therefore, Monarchs have had to develop a sense that we take for granted. Using highly specialised machinery, Monarchs are believed to be able to compensate for the effect of time on the position of the Sun and re-orientate themselves based on this information, developing what is now known as a ‘time compensated sun compass’. A series of fascinating experiments showed how important time-compensation is to migrating Monarchs. Using the apparatus shown in on the left, researchers showed that shifting the Monarchs’ body clocks, known as circadian clocks, by six hours caused the butterflies to incorrectly interpret the position of the sun and hence orientate themselves away from their migratory heading.
With the importance of the circadian clocks firmly established, attention shifted to the biological processes that underpinned this process. Explorations into the brain architecture of migratory Monarchs highlighted a self-inhibiting process, known as a negative feedback loop, that occurred in just four cells in an area known as the central complex and seemed to fit a 24-hour circadian rhythm.
It was found that in these four cells, the amounts of a set of proteins being produced oscillated over a 24-hour period. This architecture was highly similar to the one that operates in flies and seemed to rely heavily on two sets of light-sensitive proteins known as Cryptochrome (CRY). Interestingly, Monarchs are unique in their possession of an invertebrate, fly-like, CRY and a vertebrate-like CRY that is highly similar to those found in humans.
Eventually, the following interrelationship was discovered (see image below). Two proteins, appropriately named CLOCK (CLK) and CYCLE (CYC) modify the DNA in the nucleus of these cells to produce three more proteins – Cryptochrome 2, TIMELESS (TIM) and PERIOD (PER). However, the production of these proteins is relatively short-lived. In a process triggered by light, another protein, CRY1, degrades TIM and destroys it. In a beautiful circadian mechanism, the PER protein, which is attached to CRY2, is slowly modified and eventually translocates to the nucleus, where it was produced, and shuts off its own production. Once this 24-hour long process is completed, the cycle begins again. It is using this mechanism that the Monarch is able to achieve a 24-hour oscillation of the proteins its cells are producing, and hence allow for time-compensation of their detection of Sun-derived directional cues.
The mystery of Monarch migration seemed all but solved. However, researchers were shocked to discover that the machinery in the Monarch brain was not responsible for sun compass time compensation; Monarchs that lacked these proteins in the central complex were unexpectedly able to correctly orientate themselves. This lead to two questions: what did the circadian clocks in the brain do, and where were the clocks that were responsible for time compensation located?
This remarkable story will be continued tomorrow…
‘Til next time,
1. Reppert SM, Gegear RJ, Merlin C. Navigational Mechanisms of Migrating Monarch Butterflies. Trends Neurosci [Internet]. 2010 Sep 2;33(9):399–406. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2929297/
2. Zhan S, Merlin C, Boore JL, Reppert SM. The Monarch Butterfly Genome Yields Insights into Long-Distance Migration. Cell [Internet]. Elsevier; 2016 Jun 1;147(5):1171–85. Available from: http://dx.doi.org/10.1016/j.cell.2011.09.052
3. Guerra PA, Reppert SM. Sensory basis of lepidopteran migration: focus on the monarch butterfly. Curr Opin Neurobiol [Internet]. 2015 Oct;34:20–8. Available from: http://www.sciencedirect.com/science/article/pii/S0959438815000185
Image sources are given in figure legends. All rights and credit goes to original authors.