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The genetics of monarch butterfly migration and warning colouration

Abstract

The monarch butterfly, Danaus plexippus, is famous for its spectacular annual migration across North America, recent worldwide dispersal, and orange warning colouration. Despite decades of study and broad public interest, we know little about the genetic basis of these hallmark traits. Here we uncover the history of the monarch’s evolutionary origin and global dispersal, characterize the genes and pathways associated with migratory behaviour, and identify the discrete genetic basis of warning colouration by sequencing 101 Danaus genomes from around the globe. The results rewrite our understanding of this classic system, showing that D. plexippus was ancestrally migratory and dispersed out of North America to occupy its broad distribution. We find the strongest signatures of selection associated with migration centre on flight muscle function, resulting in greater flight efficiency among migratory monarchs, and that variation in monarch warning colouration is controlled by a single myosin gene not previously implicated in insect pigmentation.

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Figure 1: Global dispersal of the monarch butterfly.
Figure 2: A selective sweep associated with migration.
Figure 3: Divergent selection on collagen IV α-1.
Figure 4: The genetic basis of warning colouration.

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Accession codes

Primary accessions

Sequence Read Archive

Data deposits

Sequence data are deposited in the NCBI Short Read Archive (SRA) database (accession numbers SRP045457 and SRP045468).

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Acknowledgements

We thank B. Ballister, S. Barribeau, R. Bartel, N. Chamberlain, R. Cook, A. Davis, D. Feary, D. Frey, M. Maudsley, G. Moreira, E. Osburn, R. Rarick, E. Rendon, D. Rodrigues, E. Sternberg and J. Stimson for assistance collecting or providing specimens. We also thank J. Jensen and D. Lohman for discussion. This work was supported by National Institutes of Health grant GM086794-02S1, National Science Foundation grants IOS-134367, DEB-0643831, DEB-1019746 and DEB-1316037, start-up funds from the Chinese Academy of Sciences and Shanghai Institutes for Biological Sciences, and Neubauer Funds from the University of Chicago.

Author information

Authors and Affiliations

Authors

Contributions

S.Z. designed and implemented analyses of dispersal and migration and co-wrote the manuscript. W.Z. performed wing colour analyses. K.N. performed respirometry experiments. J.H. helped design the project and collected and prepared samples for sequencing. J.F.H. and M.P.Z. provided samples and interpreted results. S.A., J.C.d.R. and S.M.R. helped design the project, provided samples, and interpreted results. M.R.K. conceived and directed the project, performed targeted population genetic analyses, and co-wrote the manuscript.

Corresponding authors

Correspondence to Shuai Zhan or Marcus R. Kronforst.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Relationships among monarch populations inferred using the maximum likelihood method implemented in Treemix.

Note, this is a fully resolved, bifurcating tree. The very short basal branches indicate little genetic drift in North American populations, not unresolved basal relationships. Colours correspond to those in Fig. 1. Treemix also inferred five migration events among populations: from Puerto Rico to Aruba, from Puerto Rico to Costa Rica, from New Caledonia to Fiji, from Belize or Costa Rica to Portugal, and from Belize to Puerto Rico.

Extended Data Figure 2 Demographic history of the monarch butterfly.

a, Patterns of linkage-disequilibrium decay across the genome in different geographic populations. b, Genome-wide distribution of minor allele frequencies. c, Heterozygosity across populations, estimated as the ratio of heterozygous SNPs to homozygous SNPs/individual. d, Demographic history inferred using PSMC. This analysis includes representative individuals of high sequencing depth for each geographic location. The period of the last glacial maximum (LGM; 20,000 years ago) is shaded in grey.

Extended Data Figure 3 ∂a∂i analysis parameter estimates.

a, Schematic of demographic scenario modelled in ∂a∂i labelled with parameters being estimated. Nu, effective population size (individuals); m, migration rate (individuals/year); T, time (years). b, Inferred parameter estimates. c, One-dimensional model-data comparison considering North America population only. In the left panel, the model is plotted in red and the data in blue. In the right panel, the residuals between model and data are plotted. d, Two-dimensional comparison for joint estimation of North America and dispersal populations (Central/South America, Pacific, Atlantic). The left two panels are marginal spectra for data and the maximum-likelihood model, respectively. The right two panels show the residuals.

Extended Data Table 1 Inferring the monarch range expansion
Extended Data Table 2 Top 20 migration-associated genomic regions

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Zhan, S., Zhang, W., Niitepõld, K. et al. The genetics of monarch butterfly migration and warning colouration. Nature 514, 317–321 (2014). https://doi.org/10.1038/nature13812

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