Studies of the migration of the eastern North American monarch butterfly () have revealed mechanisms behind its navigation. The main orientation mechanism uses a time-compensated sun compass during both the migration south and the remigration north. Daylight cues, such as the sun itself and polarized light, are processed through both eyes and integrated through intricate circuitry in the brain's central complex, the presumed site of the sun compass. Monarch circadian clocks have a distinct molecular mechanism, and those that reside in the antennae provide time compensation. Recent evidence shows that migrants can also use a light-dependent inclination magnetic compass for orientation in the absence of directional daylight cues. The monarch genome has been sequenced, and genetic strategies using nuclease-based technologies have been developed to edit specific genes. The monarch butterfly has emerged as a model system to study the neural, molecular, and genetic basis of long-distance animal migration.


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Literature Cited

  1. Allada R, Chung BY. 1.  2010. Circadian organization of behavior and physiology in Drosophila. Annu. Rev. Physiol. 72:605–24 [Google Scholar]
  2. Bélles X, Martín D, Piulachs MD. 2.  2005. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu. Rev. Entomol. 50:181–99 [Google Scholar]
  3. Brower LP. 3.  1995. Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857–1995. J. Lepid. Soc. 49:304–85 [Google Scholar]
  4. Brower LP, Taylor OR, Williams EH, Slayback DA, Zubieta RR. 4.  et al. 2012. Decline of monarch butterflies overwintering in Mexico: Is the migratory phenomenon at risk?. Insect Conserv. Divers. 5:95–100 [Google Scholar]
  5. Calvert WH. 5.  2001. Monarch butterfly (Danaus plexippus L., Nymphalidae) fall migration: flight behavior and direction in relation to celestial and physiographic cues. J. Lepid. Soc. 55:162–68 [Google Scholar]
  6. Carlsson MA, Schäpers A, Nässael DR, Janz N. 6.  2013. Organization of the olfactory system of Nymphalidae butterflies. Chem. Senses 38:355–67 [Google Scholar]
  7. Dieudonné A, Daniel TL, Sane EP. 7.  2014. Encoding properties of the mechanosensory neurons in the Johnston's organ of the hawk moth, Manduca sexta. J. Exp. Biol. 217:3045–56 [Google Scholar]
  8. Dingle H. 8.  2014. Migration: The Biology of Life on the Move Oxford, UK: Oxford Univ. Press [Google Scholar]
  9. Dingle H, Zalucki MP, Rochester WA, Armijo-Prewitt T. 9.  2005. Distribution of the monarch butterfly, Danaus plexippus (L.) (Lepidoptera: Nymphalidae), in western North America. Biol. J. Linn. Soc. 85:491–500 [Google Scholar]
  10. el Jundi B, Pfeiffer K, Heinze S, Homberg U. 10.  2014. Integration of polarization and chromatic cues in the insect sky compass. J. Comp. Physiol. A 200:575–89 [Google Scholar]
  11. Engels S, Schneider NL, Lefeldt N, Hein CM, Zapka M. 11.  et al. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509:353–56 [Google Scholar]
  12. Flatt T, Tu MP, Tatar M. 12.  2005. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27:999–1010 [Google Scholar]
  13. Froy O, Gotter AL, Casselman AL, Reppert SM. 13.  2003. Illuminating the circadian clock in monarch butterfly migration. Science 300:1303–5 [Google Scholar]
  14. Fuller SB, Straw AD, Peek MY, Murray RM, Dickinson MH. 14.  2014. Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae. PNAS 111:E1182–91 [Google Scholar]
  15. Gaj T, Gersbach CA, Barbass CF III. 15.  2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405 [Google Scholar]
  16. Gegear RJ, Casselman A, Waddell S, Reppert SM. 16.  2008. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454:1014–18 [Google Scholar]
  17. Gegear RJ, Foley LE, Casselman A, Reppert SM. 17.  2010. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463:804–7 [Google Scholar]
  18. Gibo DL. 18.  1986. Flight strategies of migrating monarch butterflies (Danaus plexippus L.) in southern Ontario. Insect Flight, Dispersal and Migration W Danthanarayana 172–84 Berlin: Springer-Verlag [Google Scholar]
  19. Gibo DL, Pallett MJ. 19.  1979. Soaring flight of monarch butterflies, Danaus plexippus (Lepidoptera, Danaidae), during the late summer migration in southern Ontario. Can. J. Zool. 57:1393–401 [Google Scholar]
  20. Goehring L, Oberhauser KS. 20.  2002. Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus. Ecol. Entomol. 27:674–85 [Google Scholar]
  21. Grishin NV. 21.  2014. Why the monarch butterfly should not be listed under the Endangered Species Act. News Lepid. Soc. 56:193–96 [Google Scholar]
  22. Guerra PA, Gegear RJ, Reppert SM. 22.  2014. A magnetic compass aids monarch butterfly migration. Nat. Commun. 5:4164 [Google Scholar]
  23. Guerra PA, Merlin C, Gegear RJ, Reppert SM. 23.  2012. Discordant timing between antennae disrupts sun compass orientation in migratory monarch butterflies. Nat. Commun. 3:958 [Google Scholar]
  24. Guerra PA, Reppert SM. 24.  2013. Coldness triggers northward flight in remigrant monarch butterflies. Curr. Biol. 23:419–23 [Google Scholar]
  25. Guerra PA, Reppert SM. 25.  2015. Sensory basis of lepidopteran migration: focus on the monarch butterfly. Curr. Opin. Neurobiol. 34:20–28 [Google Scholar]
  26. Guilford T, Taylor GK. 26.  2014. The sun compass revisited. Anim. Behav. 97:135–43 [Google Scholar]
  27. Heinze S, Florman J, Asokaraj S, el Jundi B, Reppert SM. 27.  2013. Anatomical basis of sun compass navigation II: the neuronal composition of the central complex of the monarch butterfly. J. Comp. Neurol. 521:267–98 [Google Scholar]
  28. Heinze S, Reppert SM. 28.  2011. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–58 [Google Scholar]
  29. Heinze S, Reppert SM. 29.  2012. Anatomical basis of sun compass navigation I: the general layout of the monarch butterfly brain. J. Comp. Neurol. 520:1599–628 [Google Scholar]
  30. Helfrich-Förster C, Täuber M, Park JH, Mühlig-Versen M, Schneuwly S. 30.  et al. 2000. Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. J. Neurosci. 20:3339–53 [Google Scholar]
  31. Herman WS. 31.  1975. Endocrine regulation of posteclosion enlargement of the male and female reproductive glands in monarch butterflies. Gen. Comp. Endocrinol. 26:534–40 [Google Scholar]
  32. Herman WS, Tatar M. 32.  2001. Juvenile hormone regulation of longevity in the migratory monarch butterfly. Proc. R. Soc. B 268:2509–14 [Google Scholar]
  33. Holland RA, Wikelski M, Wilcove DS. 33.  2006. How and why do insects migrate?. Science 313:794–96 [Google Scholar]
  34. Kim H, Kim JS. 34.  2014. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15:321–34 [Google Scholar]
  35. Knight A, Brower LP. 35.  2009. The influence of Eastern North American autumnal migrant monarch butterflies (Danaus plexippus L.) on continuously breeding resident monarch populations in Southern Florida. J. Chem. Ecol. 35:816–23 [Google Scholar]
  36. Kyriacou CP. 36.  2009. Clocks, cryptochromes and monarch migrations. J. Biol. 8:55 [Google Scholar]
  37. Labhart T, Baumann F, Bernard GD. 37.  2009. Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta. Cell Tissue Res. 338:391–400 [Google Scholar]
  38. Liu Y, Ma S, Wang X, Chang J, Gao J. 38.  et al. 2014. Highly efficient multiplex targeted mutagenesis and genomic structure variation in Bombyx mori cells using CRISPR/Cas9. Insect Biochem. Mol. Biol. 49:35–42 [Google Scholar]
  39. Ma S, Zhang S, Wang F, Liu Y, Liu Y. 39.  et al. 2012. Highly efficient and specific genome editing in silkworm using custom TALENs. PLOS ONE 7:e45035 [Google Scholar]
  40. Matsuo E, Kamikouchi A. 40.  2013. Neuronal encoding of sound, gravity, and wind in the fruit fly. J. Comp. Physiol. A 199:253–62 [Google Scholar]
  41. Merlin C, Beaver LE, Taylor OR, Wolfe SA, Reppert SM. 41.  2013. Efficient targeted mutagenesis in the monarch butterfly using zinc finger nucleases. Genome Res. 23:169–80 [Google Scholar]
  42. Merlin C, Gegear RJ, Reppert SM. 42.  2009. Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies. Science 325:1700–4 [Google Scholar]
  43. Merlin C, Heinze S, Reppert SM. 43.  2012. Unraveling navigational mechanisms in migratory insects. Curr. Opin. Neurobiol. 22:353–61 [Google Scholar]
  44. Mouritsen H, Derbyshire R, Stalleicken J, Mouritsen . 44.  et al. 2013. An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators. PNAS 110:7348–53 [Google Scholar]
  45. Mouritsen H, Derbyshire R, Stalleicken J, Mouritsen . 45.  et al. 2013. Reply to Oberhauser et al.: The experimental evidence clearly shows that monarch butterflies are almost certainly not true navigators. PNAS 110:e3681 [Google Scholar]
  46. Mouritsen H, Frost BJ. 46.  2002. Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. PNAS 99:10162–66 [Google Scholar]
  47. Oberhauser KS, Taylor OR, Reppert SM, Dingle H, Nail KR. 47.  et al. Are monarch butterflies true navigators? The jury is still out. PNAS 110:e3680 [Google Scholar]
  48. Palomares LA, Joosten CE, Hughes PR, Granados RR, Shuler ML. 48.  2003. Novel insect cell line capable of complex N-glycosylation and sialylation of recombinant proteins. Biotechnol. Prog. 19:185–92 [Google Scholar]
  49. Partch CL, Green CB, Takahashi JS. 49.  2014. Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24:90–99 [Google Scholar]
  50. Perez SM, Taylor OR. 50.  2004. Monarch butterflies' migratory behavior persists despite changes in environmental conditions. The Monarch Butterfly: Biology and Conservation KS Oberhauser, MJ Solensky 85–89 Cornell, NY: Cornell Univ. Press [Google Scholar]
  51. Perez SM, Taylor OR, Jander R. 51.  1997. A sun compass in monarch butterflies. Nature 387:29 [Google Scholar]
  52. Pierce A, Zalucki MP, Bangura M, Udawatta M, Kronforst M. 52.  et al. 2014. Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proc. R. Soc. B 281:20142230 [Google Scholar]
  53. Reppert SM. 53.  2006. A colorful model of the circadian clock. Cell 124:233–36 [Google Scholar]
  54. Reppert SM, Gegear RJ, Merlin C. 54.  2010. Navigational mechanisms of migrating monarch butterflies. Trends Neurosci. 33:399–406 [Google Scholar]
  55. Reppert SM, Zhu H, White R. 55.  2004. Polarized light helps monarch butterflies navigate. Curr. Biol. 14:155–58 [Google Scholar]
  56. Reynolds AM, Reynolds DR, Smith AD, Chapman JW. 56.  2010. Orientation cues for high-flying nocturnal insect migrants: Do turbulence-induced temperature and velocity fluctuations indicate the mean wind flow?. PLOS ONE 5:e15758 [Google Scholar]
  57. Sajwan S, Takasu Y, Tamura T, Uchino K, Sezutsu H. 57.  et al. 2013. Efficient disruption of endogenous Bombyx gene by TAL effector nucleases. Insect Biochem. Mol. Biol. 431:17–23 [Google Scholar]
  58. Sauman I, Briscoe AD, Zhu H, Shi D, Froy O. 58.  et al. 2005. Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46:457–67 [Google Scholar]
  59. Schmidt-Koenig K. 59.  1979. Directions of migrating monarch butterflies (Danaus plexippus; Danaidae; Lepidoptera) in some parts of the eastern United States. Behav. Process. 4:73–78 [Google Scholar]
  60. Shafer OT, Taghert PH. 60.  2009. RNA-interference knockdown of Drosophila pigment dispersing factor in neuronal subsets: the anatomical basis of a neuropeptide's circadian functions. PLOS ONE 4:e8298 [Google Scholar]
  61. Slee M. 61.  2012. Flight of the Butterflies (film). Toronto: SK Films [Google Scholar]
  62. Stalleicken J, Labhart T, Mouritsen H. 62.  2006. Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J. Comp. Physiol. A 192:321–31 [Google Scholar]
  63. Stalleicken J, Mukhida M, Labhart T, Wehner R, Frost BJ. 63.  et al. 2005. Do monarch butterflies use polarized skylight for migratory orientation?. J. Exp. Biol. 208:2399–408 [Google Scholar]
  64. Takasu Y, Kobayashi I, Beumer K, Uchino K, Sezutsu H. 64.  et al. 2010. Targeted mutagenesis in the silkworm Bombyx mori using zinc finger nuclease mRNA injection. Insect Biochem. Mol. Biol. 4010:759–65 [Google Scholar]
  65. Thorup K, Holland RA. 65.  2009. The bird GPS—long-range navigation in migrants. J. Exp. Biol. 212:3597–604 [Google Scholar]
  66. Urquhart FA. 66.  1987. The Monarch Butterfly: International Traveler Chicago, IL: Nelson-Hall [Google Scholar]
  67. Wang Y, Li Z, Xu J, Zeng B, Ling L. 67.  et al. 2013. The CRISPR/Cas system mediates efficient genome engineering in Bombyx mori. Cell Res 2312:1414–16 [Google Scholar]
  68. Watanabe T, Ochiai H, Sakuma T, Horch HW, Hamaguchi N. 68.  et al. 2012. Non-transgenic genome modifications in a hemimetabolous insect using zinc-finger and TAL effector nucleases. Nat. Commun. 3:1017 [Google Scholar]
  69. Wiltschko W, Wiltschko R. 69.  2005. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A 191:675–93 [Google Scholar]
  70. Yuan Q, Metterville D, Briscoe AD, Reppert SM. 70.  2007. Insect cryptochromes: Gene duplication and loss define diverse ways to construct insect circadian clocks. Mol. Biol. Evol. 24:948–55 [Google Scholar]
  71. Zhan S, Merlin C, Boore JL, Reppert SM. 71.  2011. The monarch butterfly genome yields insights into long-distance migration. Cell 147:1171–85 [Google Scholar]
  72. Zhan S, Reppert SM. 72.  2013. MonarchBase: the monarch butterfly genome database. Nucleic Acids Res. 41:D1D758–63 [Google Scholar]
  73. Zhan S, Zhang W, Niitepõld K, Hsu J, Haeger F. 73.  et al. 2014. The genetics of monarch butterfly migration and warning coloration. Nature 514:317–21 [Google Scholar]
  74. Zhu H, Casselman A, Reppert SM. 74.  2008. Chasing migration genes: a brain expressed sequence tag resource for summer and migratory butterflies (Danaus plexippus). PLOS ONE 3:e1345 [Google Scholar]
  75. Zhu H, Gegear RJ, Casselman AL, Kanginakudru S, Reppert SM. 75.  2009. Defining behavioral and molecular differences between summer and migratory monarch butterflies. BMC Biol. 7:14 [Google Scholar]
  76. Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M. 76.  et al. 2008. Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLOS Biol. 6:e4 [Google Scholar]
  77. Zhu H, Yuan Q, Briscoe AD, Froy O, Casselman A. 77.  et al. 2005. The two CRYs of the butterfly. Curr. Biol. 15:R953–54 [Google Scholar]

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