Ancient DNA reveals the timing and persistence of organellar genetic bottlenecks over 3,000 years of sunflower domestication and improvement

Nathan Wales, Melis Akman, Ray H.B. Watson, Fátima Sánchez Barreiro, Bruce D. Smith, Kristen J. Gremillion, M. Thomas P. Gilbert, Benjamin K. Blackman

Research output: Contribution to journalArticlepeer-review

Abstract

Here, we report a comprehensive paleogenomic study of archaeological and ethnographic sunflower remains that provides significant new insights into the process of domestication of this important crop. DNA from both ancient and historic contexts yielded high proportions of endogenous DNA, and although archaeological DNA was found to be highly degraded, it still provided sufficient coverage to analyze genetic changes over time. Shotgun sequencing data from specimens from the Eden's Bluff archaeological site in Arkansas yielded organellar DNA sequence from specimens up to 3,100 years old. Their sequences match those of modern cultivated sunflowers and are consistent with an early domestication bottleneck in this species. Our findings also suggest that recent breeding of sunflowers has led to a loss of genetic diversity that was present only a century ago in Native American landraces. These breeding episodes also left a profound signature on the mitochondrial and plastid haplotypes in cultivars, as two types were intentionally introduced from other Helianthus species for crop improvement. These findings gained from ancient and historic sunflower specimens underscore how future in-depth gene-based analyses can advance our understanding of the pace and targets of selection during the domestication of sunflower and other crop species.

Original languageEnglish (US)
Pages (from-to)38-53
Number of pages16
JournalEvolutionary Applications
Volume12
Issue number1
DOIs
StatePublished - Jan 2019
Externally publishedYes

Bibliographical note

Funding Information:
This research was funded by the National Science Foundation (DEB-1354622, DEB-1640788) and the Danish National Research Foundation. Permission for destructive sampling of archaeological and historic materials was kindly granted by the National Museum of the American Indian, the University of Arkansas Collections Facility, The Osage Nation, and the University of Michigan Museum of Archaeological Anthropology. In particular, we acknowledge the invaluable assistance of Andrea A. Hunter, Tribal Historic Preservation Officer, Osage Nation; Mary Suter, Curator of Collections, University Museum, University of Arkansas; and Emily Kaplan, National Museum of the American Indian. We thank Filipe G. Vieira, Thorfinn Sand Korneliussen, Mikkel Schubert, Mike Martin, and Vanessa Bieker for bioinformatic advice and Shyam Gopalakrishnan, Ida Moltke, and JazmDᴀn RamMosa-drigal for thoughtful discussions. Special thanks to the Danish National High-throughput Sequencing Centre for assistance in generating Illumina data. We also thank Ke Bi and Jason Huff at the UC Berkeley Computational Genomics Resource Laboratory for their support. Thanks to members of the Blackman laboratory and two anonymous reviewers who provided comments on the manuscript. Publication made possible in part by support from the Berkeley Research Impact Initiative (BRII) sponsored by the UC Berkeley Library.

Publisher Copyright:
© 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

Keywords

  • ancient DNA
  • archaeobotany
  • domestication
  • genetic bottleneck
  • Helianthus annuus
  • paleogenomics
  • plant evolution
  • sunflower

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