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The origin and evolution of maize in the Southwestern United States

Nature Plants volume 1, Article number: 14003 (2015) Cite this article

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An Erratum to this article was published on 14 January 2015

Abstract

The origin of maize (Zea mays mays) in the US Southwest remains contentious, with conflicting archaeological data supporting either coastal1–4 or highland5,6 routes of diffusion of maize into the United States. Furthermore, the genetics of adaptation to the new environmental and cultural context of the Southwest is largely uncharacterized7. To address these issues, we compared nuclear DNA from 32 archaeological maize samples spanning 6,000 years of evolution to modern landraces. We found that the initial diffusion of maize into the Southwest about 4,000 years ago is likely to have occurred along a highland route, followed by gene flow from a lowland coastal maize beginning at least 2,000 years ago. Our population genetic analysis also enabled us to differentiate selection during domestication for adaptation to the climatic and cultural environment of the Southwest, identifying adaptation loci relevant to drought tolerance and sugar content.

Documenting ancient diffusion routes of domesticates and how they were modified when introduced into new regions has long been a challenge. For example, hybridization and gene flow have long confounded attempts to understand the origins of either indica rice8 in the Indian subcontinent or maize in southern Mexico9. The origin and adaptation of maize in the US Southwest is a similarly difficult case. Following its initial domestication from the wild grass teosinte in southern Mexico10,11, maize diffused throughout the Americas, spreading through much of the continental United States after its introduction to the Southwest around 4,100 calendar years before present (BP)7. There has been considerable debate about the arrival of maize into the Southwest, however, as early archaeological samples suggested a highland route5,6, whereas more recent samples1,2 and morphological similarity to extant Mexican maize support a lowland, Pacific coast route3,4. And while temporal variation in Southwest maize cob morphology has been described2, the genetic changes responsible for adaptation to the Southwest environment during the last 4,000 years are still uncharacterized.

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Figure 1: Origins of the Southwest ancient maize samples.
Figure 2: Potential targets of selection during domestication.
Figure 3: Timing of selective pressures on genes involved in the starch metabolism.

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Acknowledgements

The authors acknowledge the following grants: Marie Curie Actions IEF 272927 and COFUND DFF-1325-00136, Danish National Research Foundation DNRF94, Danish Council for Independent Research 10-081390 and 1325-00136, Lundbeck Foundation grant R52-A5062, Vand Fondecyt Grant 1130261, a grant from the UC Davis Genome Center for the highland maize sequence and NSF IOS-1238014. R.F. is supported by a Young Investigator grant (VKR023446) from Villum Fonden. P.S. was funded by the Wenner-Gren foundation. The authors thank Ângela Ribeiro, Shohei Takuno and Philip Johnson for comments and discussion and staff at the Danish National High-Throughput DNA Sequencing for technical support.

Author information

Authors and Affiliations

  1. Centre for GeoGenetics, University of Copenhagen, 1350 Copenhagen, Denmark

    Rute R. da Fonseca, Nathan Wales, Enrico Cappellini, José Alfredo Samaniego, Christian Carøe, María C. Ávila-Arcos, Thorfinn Sand Korneliussen, Filipe Garrett Vieira, Eske Willerslev, Rasmus Nielsen & M. Thomas P. Gilbert

  2. The Bioinformatics Centre, University of Copenhagen, 2200 Copenhagen, Denmark

    Rute R. da Fonseca & Anders Albrechtsen

  3. Department of Anthropology, Program in Human Ecology and Archaeobiology, National Museum of Natural History, Smithsonian Institution, Washington DC 20560, USA

    Bruce D. Smith

  4. Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA

    Pontus Skoglund

  5. Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA

    Matteo Fumagalli & Filipe Garrett Vieira

  6. Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA

    María C. Ávila-Arcos

  7. Department of Ecology, Evolution, & Organismal Biology, Iowa State University, 50011, USA

    David E. Hufnagel & Matthew B. Hufford

  8. Department of Evolutionary Biology, Uppsala University, Uppsala 752 36, Sweden

    Mattias Jakobsson

  9. Science for Life Laboratory, Uppsala University, Uppsala 752 36, Sweden

    Mattias Jakobsson

  10. Instituto de Alta Investigación, Universidad de Tarapacá, 15101 Arica, Chile

    Bernardo Arriaza

  11. Department of Integrative Biology and Statistics, University of California, Berkeley, California 94720-3140, USA

    Rasmus Nielsen

  12. Department of Plant Sciences, Center for Population Biology and Genome Center, University of California, Davis, California 95616, USA

    Jeffrey Ross-Ibarra

  13. Department of Environment and Agriculture, Trace and Environmental DNA Laboratory, Curtin University, Perth, Western Australia, 6102, Australia

    M. Thomas P. Gilbert

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  1. Rute R. da Fonseca
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Contributions

M.T.P.G., B.D.S. and R.R.F. conceived and headed the project. M.T.P.G., N.W. and E.C. designed the experimental research project setup. R.R.F. designed the bioinformatics and population genetics setup with input from M.T.P.G., A.A. and J.R.I. Both B.D.S. and B.A. provided ancient samples and associated context information. M.B.H. and J.R.I. provided sequence data for the highland Palomero de Jalisco landrace. B.D.S. provided the archaeological background and performed the radiocarbon dating. N.W., E.C. and C.C. performed the ancient DNA extractions, library construction and capture with input from M.T.P.G. Both M.C.A. and J.A.S. provided bioinformatics support for the optimization of the capture-related laboratory work. J.A.S. annotated the silent and non-synonymous sites. TSK designed the tool to filter transitions in bam files. R.R.F. chose the capture targets, performed the quality filtering and mapping of the ancient datasets, and prepared the maize HapMap2 data and the modern genome data for all downstream analyses. R.R.F. performed the error determination, neutrality tests, NGSadmix, TreeMix, phylogenetic and demographic inference analyses with input from A.A. and J.R.I. D-statistics analysis was performed by P.S. with input from M.J. Both R.R.F. and M.F. performed the PBS-based selection analyses with input from R.N. Both D.E.H. and M.B.H. performed the STRUCTURE analysis. F.G.V. performed the inbreeding analysis. R.R.F., B.D.S., M.B.H., J.R.I. and M.T.P.G. wrote the manuscript with critical input from all authors.

Corresponding authors

Correspondence to Rute R. da Fonseca or M. Thomas P. Gilbert.

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da Fonseca, R., Smith, B., Wales, N. et al. The origin and evolution of maize in the Southwestern United States. Nature Plants 1, 14003 (2015). https://doi.org/10.1038/nplants.2014.3

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