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Genome editing retraces the evolution of toxin resistance in the monarch butterfly.

ABSTRACT: Identifying the genetic mechanisms of adaptation requires the elucidation of links between the evolution of DNA sequence, phenotype, and fitness1. Convergent evolution can be used as a guide to identify candidate mutations that underlie adaptive traits2-4, and new genome editing technology is facilitating functional validation of these mutations in whole organisms1,5. We combined these approaches to study a classic case of convergence in insects from six orders, including the monarch butterfly (Danaus plexippus), that have independently evolved to colonize plants that produce cardiac glycoside toxins6-11. Many of these insects evolved parallel amino acid substitutions in the ?-subunit (ATP?) of the sodium pump (Na+/K+-ATPase)7-11, the physiological target of cardiac glycosides12. Here we describe mutational paths involving three repeatedly changing amino acid sites (111, 119 and 122) in ATP? that are associated with cardiac glycoside specialization13,14. We then performed CRISPR-Cas9 base editing on the native Atp? gene in Drosophila melanogaster flies and retraced the mutational path taken across the monarch lineage11,15. We show in vivo, in vitro and in silico that the path conferred resistance and target-site insensitivity to cardiac glycosides16, culminating in triple mutant 'monarch flies' that were as insensitive to cardiac glycosides as monarch butterflies. 'Monarch flies' retained small amounts of cardiac glycosides through metamorphosis, a trait that has been optimized in monarch butterflies to deter predators17-19. The order in which the substitutions evolved was explained by amelioration of antagonistic pleiotropy through epistasis13,14,20-22. Our study illuminates how the monarch butterfly evolved resistance to a class of plant toxins, eventually becoming unpalatable, and changing the nature of species interactions within ecological communities2,6-11,15,17-19.

SUBMITTER: Karageorgi M

PROVIDER: S-EPMC7039281 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Genome editing retraces the evolution of toxin resistance in the monarch butterfly.

Karageorgi Marianthi M Groen Simon C SC Sumbul Fidan F Pelaez Julianne N JN Verster Kirsten I KI Aguilar Jessica M JM Hastings Amy P AP Bernstein Susan L SL Matsunaga Teruyuki T Astourian Michael M Guerra Geno G Rico Felix F Dobler Susanne S Agrawal Anurag A AA Whiteman Noah K NK

Nature 20191002 7778

Identifying the genetic mechanisms of adaptation requires the elucidation of links between the evolution of DNA sequence, phenotype, and fitness1. Convergent evolution can be used as a guide to identify candidate mutations that underlie adaptive traits2-4, and new genome editing technology is facilitating functional validation of these mutations in whole organisms1,5. We combined these approaches to study a classic case of convergence in insects from six orders, ...[more]

PMID: 31578524

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Project description:Elucidating the adaptations that promote flight in animals can aid the understanding of evolution and species divergence, and/or provide inspiration for aerospace engineering and the design of better aerial vehicles. The famed long-distance migration of monarch butterflies in North America still holds many questions and opportunities for inspiration. For example, there is little research on whether the monarch’s primary wing colors themselves (black, orange, or white) have any aerodynamic or migration function. Dark colors on wings of other animals have recently been shown to aid flight by enhancing solar absorption, which reduces drag forces. However, too much black surface could be problematic for monarchs, which are exposed to increasing amounts of solar energy along their flightpath. This paper describes the results of two related investigations that attempt to elucidate the importance of wing color to the monarch migration. By measuring the color proportions of nearly 400 monarch wings collected at different stages of their journey, we found, surprisingly, that successful migrants tended to have less black on their wings (about 3% less), but also more white pigment (about 3% more); monarchs have a band of light-colored marginal wing spots. Second, image analysis of museum specimens revealed migratory monarchs had significantly larger white spots, proportional to the wing area, than most non-migratory, New World Danaid butterflies, which argues spot size has evolved along with migratory behavior. Combined, these findings strongly suggest that the long-distance migration itself selects for larger white spots every fall, so that only those individuals with large spots will survive to pass on their genes. Further experimental work is needed to elucidate how the spots aid the migration, but it is possible that they enhance aerodynamic efficiency; other work by the authors demonstrates how alternating white and black pigment on wings can reduce drag. These results will serve as a useful starting point for such endeavors, which should improve understanding of one of the world’s most fascinating animal migrations, and also provide practical knowledge for the field of aerospace engineering.

Dataset Information

Genome editing retraces the evolution of toxin resistance in the monarch butterfly.

Publications

Genome editing retraces the evolution of toxin resistance in the monarch butterfly.

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