Tracing the start of monarch butterflies’ epic journey, in their genes

Monarch butterflies (Danaus plexippus) are among the most widely recognized wild creatures in North America. Their distinctive orange-and-black wings, which warn predators that the butterflies are chock full of toxins from the milkweed they eat, make them easily spotted in backyard flower beds. They’re also known for a massive annual migration, flying thousands of miles between wintering colonies in central Mexico and summer sites across the United States and Canada. More recently, it’s been discovered that female monarchs infected by parasites respond by laying their eggs on food plants that can prevent the parasite from infecting their offspring.

Monarchs are also one of the more visible victims of the massive changes humans have made to the world around us. Increased conversion of farmland to corn production has reduced the supply of milkweed, the butterflies’ only food plant, across much of the Midwest. It’s gotten so bad the number of monarchs making the annual migration back to Mexico hit a record low last year, and while things were better in 2014, a nationwide campaign to encourage planting of milkweed in home gardens is only beginning.

For all our familiarity with monarchs, we’ve known remarkably little about their evolutionary history. That’s changing rapidly now, as evidenced by a paper published last month in the journal Nature, which uses a big new genetic dataset to trace the origins of some of the monarch’s most distinctive features.

The paper’s authors, led by Shuai Zhan, and including collaborators from Shanghai to Córdoba, collected whole-genome DNA sequence data from 80 monarchs collected from across the globe: the famous migratory populations of North America, but also non-migratory monarchs in Australia, New Zealand, and Hawaii, South America, and Europe. By comparing the DNA sequences of all those butterflies to the monarch reference genome sequence, they identified some 32 million single-nucleotide polymorphism markers—single points in the genome where some butterflies carried one DNA letter, and other butterflies carried another.

A dataset like that allows some truly high-precision reconstruction of evolutionary history. First, the authors compared the data from the 80 monarchs to DNA sequences from another nine butterflies of different species in the same genus, Danaus, and from the more distantly related silk moth and Heliconius butterflies. In the resulting evolutionary tree, the migratory North American population branched out from the base of the larger cluster of monarchs, which suggests that the common ancestors of all the monarch populations were also migrants. The non-North American populations also showed signs of founder effects, the loss of genetic diversity associated with colonizing new territory.

Zhan et al 2014, Figure 1

Monarchs from the migratory North American populations are “basal” to the other monarchs in the sample. (Zhan et al. 2014: Figure 1)

The authors then scanned through the genome-wide dataset to identify regions where monarchs from the migratory population differed from the non-migratory monarchs. A single stretch of about 21,000 DNA letters emerged as the region with the strongest contrast between migrants and non-migrants, based on multiple comparison statistics—and that stretch of sequence included the genetic code for a key muscle-development protein. Muscle endurance is a big part of making the monarchs’ long migration, so it seems quite reasonable to think that these differences in DNA reflect the results of natural selection for migration. And, indeed, the authors compared the metabolic rate of migratory and non-migratory monarchs in flight and found that the migratory monarchs expended less energy doing the same amount of work.

Zhan et al (2014) figure 4a

A monarch butterfly of a different color. (Zhan et al. 2014: Figure 4a)

In addition to non-migratory monarchs, there are populations of the butterflies that have lost their orange coloration—they’re white with black stripes instead. These nivosus monarchs are found in Hawaii, and they provided another opportunity to unravel monarch’s genetic code by comparison. Similarly to the migration analysis, Zhan et al. scanned through genomic sequence data from several orange Hawaiian monarchs, several nivosus monarchs, and some individuals that were descended from matings between parents of different color forms. Again, a single gene emerged as having different sequences in the different color morphs—this one related to a gene that has been found to affect fur color in mice.

All together, Zhan and coauthors report a really impressive volume of population genetic analysis and experimental work in this single paper—I’ve just given a brief rundown. It’s a nice example of what’s possible with really high-precision genetic data, and I hope it’s the first of many population genomic studies in the monarch. This kind of data can reveal the genetic basis of the traits and behaviors that makes monarchs so unique—but they might also help us to make sure monarchs continue their hemisphere-spanning migration for many years to come.

References

Brower L.P. 1988. Avian predation on the monarch butterfly and its implications for mimicry theory, The American Naturalist, 131 (s1) S4. DOI: 10.1086/284763

Zhan S., J.L. Boore and S.M. Reppert. 2011. The monarch butterfly genome yields insights into long-distance migration, Cell, 147 (5) 1171-1185. DOI: 10.1016/j.cell.2011.09.052

Zhan S., K. Niitepõld, J. Hsu, J.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 colouration, Nature, 514 (7522) 317-321. DOI: 10.1038/nature13812

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