Monarch Navigation

The Sun Compass and the Circadian Cycle

When the monarch butterflies of North America migrate south for the winter how do they know where to go? How does a butterfly cross hundreds of miles to get to Mexico, and how does it stay oriented? The monarch accomplishes the amazing journey with the help of a unique behavioral mechanism, a sun compass. Where other migratory species utilize things like magnetic compasses, monarch butterflies have been found to utilize the position of the sun in the sky to orient themselves southwest for their southward migration. Now, this presents a clear issue, how do the butterfly account for the movement of the sun as it moves across the sky during the day? In order to account for the rising and setting of the sun throughout the day, the monarch butterfly utilizes a 24 hour circadian clock to allow it to differentially respond to the sun as the day progresses.1

In short:

  • Monarchs use a sun compass that involves its circadian rhythm
  • Possible destination beacon

There are many components to the sun compass system in the monarch butterfly, with various centers projecting to the suspected site of the sun compass, the central complex.1,4 The dorsal rim of the butterfly’s eye transduces the angle of polarized, UV light and signals the central complex, allowing the butterfly to orient itself directionally.2 The antenna of monarchs are thought to transmit a circadian clock signal to the central complex, relying on blue light and cytochrome1 to synchronize the circadian clocks in the central complex to that of the antenna.3 This process was thought to be done with just the central complex, but recent findings have clearly demonstrated the antenna play a major role in the circadian clock used in the sun compass.3 The pathways connecting these areas to the central complex are under investigation, but the current model suggests that these parts come together to create the southwestern orientation the butterfly follows for its southern migration. There is still a missing final suspected step that allows the butterflies to locate the specific oyamel tree groves that monarchs tend to nest at, with possible mechanisms involving olfactory cues given off by the trees or magnetic cues the butterflies may use to find the grove.4

The clock mechanism utilized in the sun compass, illustrated in the upper picture, is based on the heterodimers, a quaternary structure of proteins, CLOCK (CLK) and CYCLE (CYC) which help stimulate the transcription of the period (PER), timeless (TIM), and cryptochrome2 (CRY2) genes, turning them from DNA to RNA. These genes are then translated, turned from RNA into proteins, and after approximately 24 hours the CRY2 protein moves to the nucleus and inhibits the CLOCK and CYCLE based transcription. PER suspected to play a role in the movement of CRY2 to the nucleus. Cryptochrome1 (CRY1) is a circadian photoreceptor which, when it is exposed to light (the pictured lightning bolt), causes TIM to break down, allowing light to signal the clock mechanism and help to synchronize the various circadian clocks in the butterfly. The lower picture demonstrates in which areas of the butterfly these different proteins are found. Cells expressing TIM, PER, CRY1 or CRY2 are highlighted in blue. All four clock proteins are found in two of the four cells in the each of the pars lateralis (PL). These four cells in the PL serve as the complete circadian clock cells in the butterfly brain. CRY1 cells and the connections they make are represented by green dots and green lines, respectively. Projections from the dorsal rim area photoreceptors are indicated by the dotted gold lines. Neurons and fibers expressing exclusively CRY2 are represented in red. 1,4

These mechanisms of light reception and circadian clock both signal the central complex which, as the suspected area of the sun compass, then signals the motor cortex of the butterfly and causes it to fly towards it migration destination. There are still many assumptions and unknowns within the sun compass mechanism, with the projections connecting each area to the central complex being uncertain. Current research continues to look at more of this complicated and multifaceted navigation system and many current assumptions could be overturned before an acceptable final model is of the sun compass is made.

Sun Compass 11,4

Model of the components and potential circuitry involved in the time-compensated sun compass mechanism. (Left) Skylight input to the eye: skylight cues provide directional information that is sensed by the eye and ultimately integrated into the central complex (CC), the presumed site of the sun compass. The dorsal rim area of the eye senses the angle of plane-polarized, ultraviolet light (small violet circle with crosshatches), whereas the main retina senses color gradients (small filled violet circle, small blue circle, and small green circle) or senses the sun itself (i.e. does not discriminate between the three colors). Multicircuit pathways, yet to be defined, connect eye-sensed skylight information to the central complex (dashed black and grey lines with question mark). (Right) Clock entrainment: skylight in the blue range directly entrains (synchronizes) circadian clocks in the antennae and brain to the 24 h day through direct light action on CRYPTOCHROME1. An as yet unknown neural pathway connects antennal clocks to the central complex (thick dashed red line with question mark); this is a major pathway providing timing information to the central complex. A neural pathway that connects clock cells in the pars lateralis (PL; blue spots) area of the brain to the central complex (thin dashed red line) is likely to exist; this could provide a minor pathway for timing sun compass orientation. (Below) Signal integration: information from the sun compass and circadian clock is integrated in the central complex itself or in its output pathways. Central complex output pathways communicate with the motor system to ultimately control continuous flight in the southwesterly direction.

Sun Compass 21,4,5

The main gear of the clock mechanism is an autoregulatory transcription feedback loop in which CLOCK (CLK) and CYCLE (CYC) heterodimers drive the transcription of the period (per), timeless (tim), and cryptochrome2 (cry2)genes through E box enhancer elements. TIM (T), PER (P), and CRY2 (C2) are translated and form complexes in the cytoplasm; 24 h later CRY2 is shuttled into the nucleus to inhibit CLK:CYC-mediated transcription. PER is progressively phosphorylated and probably helps to translocate CRY2 into the nucleus. CRYPTOCHROME1 (CRY1, C1) is a circadian photoreceptor which, upon light exposure (lightning bolt), causes TIM degradation, allowing light to gain access to the central clock mechanism for photic entrainment.

Steering southerly is sufficient for the bulk of the migrating monarch's travels. As millions of butterflies begin to approach Texas they are funneled together by two barriers – the Gulf of Mexico on their left and the Rocky Mountains/Sierra Madre Orientals on their right [10] (Figure 1B). However, once the butterflies continue to approach their destination, how do they find their way to the same grove in Michoacán year after year? We postulate that there is a ‘destination beacon’ that guides the butterflies to this forest. The nature of the destination beacon is not yet known but could involve olfactory cues given off at the overwintering sites by the oyamel trees that reside in the unique pine forest in which the butterflies roost or magnetic cues from field anomalies that occur there [64]. The precise nature of the destination signal is a crucial piece of the migration puzzle that needs to be solved.

Citations:

  1. Zhu, H., Sauman, I., Yuan, Q., Casselman, A., Emery-Le, M., Emery, P. and Reppert, S. M. (2008). Cryptochromes Define a Novel Circadian Clock Mechanism in Monarch Butterflies That May Underlie Sun Compass Navigation. Plos Biology, 6(1), e4. doi:10.1371/journal.pbio.0060004
  2. O. Froy, Anthony L. Gotter, Amy L. Casselman, Steven M. Reppert (2003). Illuminating the Circadian Clock in Monarch Butterfly Migration. Science, 300(5623), 1303-1305. doi:10.1126/science.1084874
  3. Merlin, C., Gegear, R., & Reppert, S. (2009). Antennal Circadian Clocks Coordinate Sun Compass Orientation in Migratory Monarch Butterflies. Science, 325(5948), 1700-1704. doi:10.1126/science.1176221
  4. Reppert, S. M., Gegear, R. J., and Merlin, C. (2010). Navigational mechanisms of migrating Monarch butterflies. Trends Neurosci. 33, 399–406. doi: 10.1016/j.tins.2010.04.004
  5. C.P. Kyriacou (2009). Clocks, cryptochromes and Monarch migrations. J. Biol., 8 (2009), p. 55