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Massive haplotypes underlie ecotypic differentiation in sunflowers

Author

Listed:
  • Marco Todesco

    (University of British Columbia
    University of British Columbia)

  • Gregory L. Owens

    (University of British Columbia
    University of British Columbia
    University of California, Berkeley)

  • Natalia Bercovich

    (University of British Columbia
    University of British Columbia)

  • Jean-Sébastien Légaré

    (University of British Columbia
    University of British Columbia
    University of British Columbia
    University of British Columbia)

  • Shaghayegh Soudi

    (University of Calgary)

  • Dylan O. Burge

    (University of British Columbia
    University of British Columbia)

  • Kaichi Huang

    (University of British Columbia
    University of British Columbia)

  • Katherine L. Ostevik

    (Duke University)

  • Emily B. M. Drummond

    (University of British Columbia
    University of British Columbia)

  • Ivana Imerovski

    (University of British Columbia
    University of British Columbia)

  • Kathryn Lande

    (University of British Columbia
    University of British Columbia)

  • Mariana A. Pascual-Robles

    (University of British Columbia
    University of British Columbia)

  • Mihir Nanavati

    (University of British Columbia
    Microsoft Research)

  • Mojtaba Jahani

    (University of British Columbia
    University of British Columbia)

  • Winnie Cheung

    (University of British Columbia
    University of British Columbia)

  • S. Evan Staton

    (University of British Columbia
    University of British Columbia)

  • Stéphane Muños

    (LIPM, Université de Toulouse, INRAE, CNRS)

  • Rasmus Nielsen

    (University of California, Berkeley)

  • Lisa A. Donovan

    (University of Georgia)

  • John M. Burke

    (University of Georgia)

  • Sam Yeaman

    (University of Calgary)

  • Loren H. Rieseberg

    (University of British Columbia
    University of British Columbia)

Abstract

Species often include multiple ecotypes that are adapted to different environments1. However, it is unclear how ecotypes arise and how their distinctive combinations of adaptive alleles are maintained despite hybridization with non-adapted populations2–4. Here, by resequencing 1,506 wild sunflowers from 3 species (Helianthus annuus, Helianthus petiolaris and Helianthus argophyllus), we identify 37 large (1–100 Mbp in size), non-recombining haplotype blocks that are associated with numerous ecologically relevant traits, as well as soil and climate characteristics. Limited recombination in these haplotype blocks keeps adaptive alleles together, and these regions differentiate sunflower ecotypes. For example, haplotype blocks control a 77-day difference in flowering between ecotypes of the silverleaf sunflower H. argophyllus (probably through deletion of a homologue of FLOWERING LOCUS T (FT)), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, frequently associated with structural variants and often appear to represent introgressions from other—possibly now-extinct—congeners. These results highlight a pervasive role of structural variation in ecotypic adaptation.

Suggested Citation

  • Marco Todesco & Gregory L. Owens & Natalia Bercovich & Jean-Sébastien Légaré & Shaghayegh Soudi & Dylan O. Burge & Kaichi Huang & Katherine L. Ostevik & Emily B. M. Drummond & Ivana Imerovski & Kathry, 2020. "Massive haplotypes underlie ecotypic differentiation in sunflowers," Nature, Nature, vol. 584(7822), pages 602-607, August.
    • Handle: RePEc:nat:nature:v:584:y:2020:i:7822:d:10.1038_s41586-020-2467-6
    DOI: 10.1038/s41586-020-2467-6
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    Cited by:

    1. Rishi De-Kayne & Oliver M. Selz & David A. Marques & David Frei & Ole Seehausen & Philine G. D. Feulner, 2022. "Genomic architecture of adaptive radiation and hybridization in Alpine whitefish," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Xuezhu Liao & Dejin Xie & Tingting Bao & Mengmeng Hou & Cheng Li & Bao Nie & Shichao Sun & Dan Peng & Haixiao Hu & Hongru Wang & Yongfu Tao & Yu Zhang & Wei Li & Li Wang, 2024. "Inversions encounter relaxed genetic constraints and balance birth and death of TPS genes in Curcuma," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Jessen V. Bredeson & Jessica B. Lyons & Ibukun O. Oniyinde & Nneka R. Okereke & Olufisayo Kolade & Ikenna Nnabue & Christian O. Nwadili & Eva Hřibová & Matthew Parker & Jeremiah Nwogha & Shengqiang Sh, 2022. "Chromosome evolution and the genetic basis of agronomically important traits in greater yam," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Tuomas Hämälä & Christopher Moore & Laura Cowan & Matthew Carlile & David Gopaulchan & Marie K. Brandrud & Siri Birkeland & Matthew Loose & Filip Kolář & Marcus A. Koch & Levi Yant, 2024. "Impact of whole-genome duplications on structural variant evolution in Cochlearia," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Thomas Dorey & Léa Frachon & Loren H. Rieseberg & Julia M. Kreiner & Florian P. Schiestl, 2024. "Biotic interactions promote local adaptation to soil in plants," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Gabriela Montejo-Kovacevich & Joana I. Meier & Caroline N. Bacquet & Ian A. Warren & Yingguang Frank Chan & Marek Kucka & Camilo Salazar & Nicol Rueda-M & Stephen H. Montgomery & W. Owen McMillan & Kr, 2022. "Repeated genetic adaptation to altitude in two tropical butterflies," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Patrik Nosil & Zachariah Gompert & Daniel J. Funk, 2024. "Divergent dynamics of sexual and habitat isolation at the transition between stick insect populations and species," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Zihao Wang & Wenxi Wang & Xiaoming Xie & Yongfa Wang & Zhengzhao Yang & Huiru Peng & Mingming Xin & Yingyin Yao & Zhaorong Hu & Jie Liu & Zhenqi Su & Chaojie Xie & Baoyun Li & Zhongfu Ni & Qixin Sun &, 2022. "Dispersed emergence and protracted domestication of polyploid wheat uncovered by mosaic ancestral haploblock inference," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Paul Battlay & Jonathan Wilson & Vanessa C. Bieker & Christopher Lee & Diana Prapas & Bent Petersen & Sam Craig & Lotte Boheemen & Romain Scalone & Nissanka P. Silva & Amit Sharma & Bojan Konstantinov, 2023. "Large haploblocks underlie rapid adaptation in the invasive weed Ambrosia artemisiifolia," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Maksim S. Makarenko & Vera A. Gavrilova, 2023. "NGS Reads Dataset of Sunflower Interspecific Hybrids," Data, MDPI, vol. 8(4), pages 1-5, March.

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