http://www.enn.com/wildlife/article/28857
Published January 8, 2008 09:15 AM


  Scientists discover molecular basis of monarch butterfly migration

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Since its discovery, the annual migration of eastern North American 
monarch butterflies has captivated the human imagination and spirit. 
That millions of butterflies annually fly a few thousand miles to reach 
a cluster of pine groves in central Mexico comprising just 70 square 
miles is, for many, an awesome and mysterious occurrence. However, over 
the past two decades, scientists have begun to unveil the journey for 
what it is: a spectacular result of biology, driven by an intricate 
molecular mechanism in a tiny cluster of cells in the butterfly brain.

University of Massachusetts Medical School Professor and Chair of 
Neurobiology Steven M. Reppert, MD, has been a pioneering force in the 
effort to demystify the migration of the monarch. His previous research 
has demonstrated that the butterflies use a time-compensated sun compass 
and daylight cues to help them navigate to the pine groves. His studies 
have shown that time compensation is provided by the butterfly's 
circadian clock, which allows the monarch to continually correct its 
flight direction to maintain a fixed flight bearing even as the sun 
moves across the sky.

Now, in two papers that will be published this week in two journals of 
the open-access publisher Public Library of Science (PLoS), Dr. Reppert 
and colleagues describe in detail the monarch butterfly circadian clock 
for the first time, and identify and characterize an entirely new clock 
gene that provides insight into not only the biology of the butterfly 
and its migration, but also the evolution of circadian clocks in general.

In "Cryptochromes Define a Novel Circadian Clock Mechanism in Monarch 
Butterflies That May Underlie Sun Compass Navigation," published in PLoS 
Biology, Reppert and colleagues reveal that the circadian clock of the 
monarch uses a novel molecular mechanism, heretofore not found in any 
other insect or mammal.

By studying the clock in two other organisms,the fruit fly and the 
mouse,scientists thought that they had very good models for an 
understanding of the insect clock and the mammalian clock, respectively. 
Through these studies, scientists had described a clock mechanism that 
is essentially a loop where proteins are made and destroyed over a cycle 
that takes approximately 24 hours to complete. Further, investigators 
identified those factors that work together to drive this process.

Reppert and colleagues were particularly interested in one of these 
factors: CRY, a cryptochrome protein that was initially discovered in 
plants and was subsequently found in the fly and the mouse. In the fly, 
CRY functions as a blue light photoreceptor, allowing light access to 
clock-containing cells. This enables the resetting of the clock by the 
light-dark cycle. In the mouse, CRY does not function to absorb light; 
rather, it is one of the essential components that power the central 
clockwork enabling the feedback loop to continue. (In the mouse, light 
enters the clock through the animal's eyes.)

Given the function of CRY in flies and the role of light in migration, 
scientists presumed that the monarch's clock would resemble that of the 
fly. Reppert and his collaborators were stunned and elated to find that 
the clock of the butterfly was as spectacular as its migration. Genetic 
studies revealed that the monarch had not only the fly-like CRY, but 
also another cryptochrome that further tests identified as a new clock 
molecule in the butterfly. Surprisingly, this cryptochrome, dubbed CRY2, 
is more similar in structure to vertebrate CRY than to that of the fruit 
fly.

Notably, the scientists also found that the core components of the 
monarch clock resembled those of the mammalian clock. As in the mouse, 
CRY2 functions in the butterfly to maintain the feedback loop, while 
CRY1 still allows light to access the cells, as in the fly.

"This is a very interesting realignment of how one thinks about insect 
clock models. There was no reason to suspect that the butterfly clock 
would be different from that of Drosophila. That it is different has 
already told us something about how circadian clocks have evolved," 
explained Reppert. "What we have in the butterfly is an astounding clock 
mechanism, one that is more similar to our own circadian clock and less 
similar to the clock of the fly! The presence and function of two 
distinct CRYs suggest that the monarch's is an ancestral clock; a clock 
that, over the course of evolution, has changed differently in other 
insects and mammals."

Reppert and colleagues not only discovered the function of CRY2 in the 
monarch clock, but they also found that CRY2 may function to mark a 
critical neural pathway from the circadian clock to the sun compass. 
This clock-to-compass pathway provides an essential link between the 
clock and the sun compass, as both are necessary for successful 
orientation and navigation. As Reppert explains, "CRY2 appears to have a 
dual function as a core clock component and as an output molecule, 
linking the clock to the compass."

Concurrent with their studies of the monarch clock and relevant to the 
identification of CRY2, Reppert and colleagues have been working to 
create a butterfly genomics resource.

In "Chasing Migration Genes: A Brain Expressed Sequence Tag Resource for 
Summer and Migratory Monarch Butterflies (Danaus plexippus)," published 
in PLoS ONE, Reppert and his collaborators describe a brain expressed 
sequence tag (EST) resource, used to identify genes involved in 
migratory behaviors by comparing the gene expression in the brains of 
migrating butterflies to those of non-migrating butterflies. They have 
already identified ~10,000 ESTs that likely represent over 50 percent of 
the genes that make up the monarch genome. The ESTs, which represent 
expression units of genes in the butterfly brain, are currently being 
analyzed and catalogued and Reppert hopes that the genetic information 
will be of wide use to scientists around the world.

"This information, along with genetic markers identified in the study, 
will help us distinguish genetic differences between populations or even 
between butterflies that are migratory and not migratory" Reppert said, 
adding, "This information sets the stage for the cloning of the 
butterfly genome."

In fact, Reppert and his fellow investigators recently initiated a 
collaborative agreement with SymBio Corporation (www.sym-bio.com) of 
Menlo Park, CA to sequence the entire butterfly genome. According to 
Robert A. Feldman, President and CEO of SymBio, "We are very excited 
about the prospect of sequencing the monarch genome. The information 
gained will not only help elucidate the molecular basis of butterfly 
migration, but will also add substantial knowledge to comparative 
genomic studies." SymBio specializes in sequencing the genomes of a wide 
range of organisms, from bacteria to mammals.

Ultimately, the Reppert laboratory will continue to work to understand 
how the monarch clock "talks" to the sun compass, with a focus on CRY2. 
The goal of the researchers' studies is to understand the molecular 
mechanism and anatomical mechanisms for clock-compass interactions that 
enable migrants to maintain a set flight bearing as the sun moves across 
the sky during the day.

Dr. Reppert also states, "The monarch provides a fascinating animal 
model for the study of neurobiology. By understanding more about the way 
the circadian clock and the sun compass interact to allow the monarch to 
fulfill its biological destiny, we will gain valuable insights into how 
the brain functions to incorporate information about time and space, 
which has relevance far beyond the butterfly."

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Kent McFarland
Vermont Center for Ecostudies
PO Box 420 • Norwich, VT 05055
802.649.1431
http://www.vtecostudies.org/