The genomic basis of the plant island syndrome in Darwin’s giant daisies

José Cerca*, Bent Petersen, José Miguel Lazaro-Guevara, Angel Rivera-Colón, Siri Birkeland, Joel Vizueta, Siyu Li, Qionghou Li, João Loureiro, Chatchai Kosawang, Patricia Jaramillo Díaz, Gonzalo Rivas-Torres, Mario Fernández-Mazuecos, Pablo Vargas, Ross A. McCauley, Gitte Petersen, Luisa Santos-Bay, Nathan Wales, Julian M. Catchen, Daniel MachadoMichael D. Nowak, Alexander Suh, Neelima R. Sinha, Lene R. Nielsen, Ole Seberg, M. Thomas P. Gilbert, James H. Leebens-Mack, Loren H. Rieseberg, Michael D. Martin*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

The repeated, rapid and often pronounced patterns of evolutionary divergence observed in insular plants, or the ‘plant island syndrome’, include changes in leaf phenotypes, growth, as well as the acquisition of a perennial lifestyle. Here, we sequence and describe the genome of the critically endangered, Galápagos-endemic species Scalesia atractyloides Arnot., obtaining a chromosome-resolved, 3.2-Gbp assembly containing 43,093 candidate gene models. Using a combination of fossil transposable elements, k-mer spectra analyses and orthologue assignment, we identify the two ancestral genomes, and date their divergence and the polyploidization event, concluding that the ancestor of all extant Scalesia species was an allotetraploid. There are a comparable number of genes and transposable elements across the two subgenomes, and while their synteny has been mostly conserved, we find multiple inversions that may have facilitated adaptation. We identify clear signatures of selection across genes associated with vascular development, growth, adaptation to salinity and flowering time, thus finding compelling evidence for a genomic basis of the island syndrome in one of Darwin’s giant daisies.

Original languageEnglish
Article number3729
JournalNature Communications
Volume13
Number of pages13
ISSN2041-1723
DOIs
Publication statusPublished - 2022

Bibliographical note

Funding Information:
J.Ce. is grateful to Simen R. Sandve for fruitful discussion and Martin LaForest for sharing genome annotations. We thank Henning Adsersen for the botanical expertise and logistical support that enabled use of the University of Copenhagen botanical collections. Jennifer Mandel kindly shared the Asteraceae COS. The collection and photography of specimens, and the preparation of this manuscript, benefited enormously from the cooperative assistance of the personnel of the Charles Darwin Foundation Research Station, who made arrangements for collecting trips, arranged laboratory space, and offered encouragement and support throughout the project. Scalesia specimens were initially collected under Galápagos National Park research permit number PC-001/98 PNG and were further normalised via Ecuador Ministry of the Environment genetic permit number MAAE-DBI-CM-2021-0213. This publication is contribution number 2426 of the Charles Darwin Foundation for the Galápagos Islands. This work was supported by the Norwegian Research Council via project number 287327 awarded to M.D.M., and a travel grant (project number 287327) granted to J.Ce. and M.D.M.

Publisher Copyright:
© 2022, The Author(s).

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