Box Extension 18.2

Migratory Navigation in Monarch Butterflies: Sensory and Genomic Information

We think of vertebrates such as fish, turtles, birds, and mammals as champion long-distance migrants, but insects such as butterflies and moths also migrate long distances (as much as 4000 km), despite their small sized and apparently flimsy bodies. Monarch butterflies (Danaus plexippus) provide a spectacular example of seasonal long-range migration. As we have discussed, their navigation cannot be learned, because the annual cycle of northward spring migration and southward fall migration involves different generations. Fall migrants are born in the north and navigate to their restricted overwintering sites that their great grandparents and great-great-grandparents left the previous winter (Figure A).

Figure A Fall migration routes of monarch butterflies. Because fall migrants were born in the north and live less that a year, they are all migrating south for the first time and cannot have learned the migration route.

The physiological and genetic basis of monarch migration, and especially the sensory basis of the navigation that underlies it, have been clarified in an ongoing series of experiments. Box extension 18.2 shows that migrating monarch butterflies use a time-compensated sun compass and a magnetic compass in migratory navigation, as well as information about daylength, wind, and temperature in controlling and modulating migratory behavior. Genomic analysis is beginning to show the genetic underpinnings of this migratory performance.

Monarch butterflies, like mammals, have circadian clocks at different locations in their bodies, and these clocks play different roles in migration. The seasonal timing of migration depends on measures of day length, using the eyes and the circadian clocks in the brain. Other circadian clocks in the antennae, in contrast, are used in orientation. The principal means of orientation is by a sun compass, as described in the book on page 503. Sun-compass navigation in monarchs is time-compensated, meaning that the position of the sun (and of associated polarized sky light) is referenced to the time of day, measured by the antennal circadian clock. Like pigeons (see Figure 18.5 in the book), monarchs mis-orient on sunny days after a clock shift (Figure B).

Figure B Sun-compass navigation in monarch butterflies is time-compensated. (1) Flight simulation chamber for measuring orientation. (2) Flight orientation of normal butterflies (above) and of time-shifted butterflies (below). The chamber is seen from above; each point is the mean flight orientation of one butterfly. All butterflies were tested at 10AM, when the sun (yellow disk) was in the southeast. The normal group oriented to the southwest, 90° from the sun (top). Butterflies that were time-shifted by 6 hours interpreted the time as 4PM, when the sun would be in the southwest, so their orientation was in error by 90°.

Fall-migrant monarchs are able to orient on overcast days, in the normal south or southwest direction. They have a magnetic sensory capability, located in the antennae, that acts as a compass. The detection of Earth’s magnetic field depends on the angle of inclination, and the monarchs interpret the direction of downward magnetic lines of force as north (Figure C, part 1; see also Figure 18.8 in the book). The ability of monarch butterflies to use magnetic fields for navigation can be tested in a flight simulator like that shown in Figure B, with the addition of a surrounding magnetic coil system (see Figure A in Box Extension 18.1). In a normal magnetic field, fall monarchs orient to the south (Figure C, part 2, top), but when the inclination of the field (dip angle) is reversed (from +45º to –45º) they orient to the north (Figure C, part 2, bottom). The inclination magnetic compass of monarchs requires blue or ultraviolet light, and appears to depend on radical-pair photochemistry, using the molecule cryptochrome (see Box Extension 18.1 for mechanism).

Figure C Magnetic field orientation of monarch butterflies in the absence of solar information. Butterflies were tested in fall, in a flight simulator like that in B, but with Helmholtz coils to alter the magnetic field. With a nornal magnetic field of + 45° the butterflies oriented to the south, but in a reversed field (- 45°) their orientation was reversed and they headed north. Arrows show mean orientation direction of the group, and dshed lines give 95% confidence interval.

The same compass mechanisms are used for southward migration in fall and for northward migration in spring. How does the “correct” direction get reversed while the butterflies are overwintering? Recent studies show that the trigger for reversing the direction of sun-compass orientation in monarchs is cold temperature. Holding fall monarchs in the cold is sufficient to trigger reversal from southward to northward. Moreover, monarchs captured in the fall and held without cold exposure until spring, continue to orient southward in the spring. Thus cold exposure seems both necessary and sufficient to reverse the direction of sun-compass-mediated migratory orientation.

Genomic differences between migrant and nonmigrant monarch butterflies

Monarch butterflies now have a broad distribution in North America, Central and South America, East Asia, and Europe. The North American populations undergo seasonal migrations, but most of the others do not. A recent study compared the genomes of 101 Danaus butterflies to find genes associated with migratory behavior. Results indicated that the North American migratory population was ancestral and that the other populations were derived from it. Interestingly, the strongest genomic signatures of migration were genes associated with flight muscle function, suggesting that flight muscle efficiency was selected for in migratory populations. Migratory monarchs had lower metabolic rates in flight than did nonmigratory monarchs. The investigators concluded that “the extreme distances required of monarch migration seem to have generated natural selection for reduced flight metabolism.” This result is analogous to reasoning, “if you are going to drive across the country, select a car with good gas mileage.”

Such studies, although still preliminary, promise to continue to clarify the genetic basis of an inherited complex behavior.

References

Guerra, P. A., and S. M. Reppert. 2013. Coldness triggers northward flight in remigrant monarch butterflies. Curr. Biol. 23: 419–423.

Guerra, P. A., and S. M. Reppert. 2015. Sensory basis of lepidopteran migration: focus on the monarch butterfly. Curr. Opin. Neurobiol. 34: 20–28.

Reppert S. M., R. J. Gegear, and C. Merlin. 2010. Navigational mechanisms in migrating monarch butterflies. Trends Neurosci. 33: 399–406.

Zhan, S., W. Zhang, K. Niitepõld, J. Hsu, F. Haeger, M. P. Zalucki, S. Altizer, J. C. de Roode, S. M. Reppert, and M. R. Kronforst. 2014. The genetics of monarch butterfly migration and warning coloration. Nature 514: 317–321.