Archaeological Central American Maize Genomes Suggest Ancient Gene Flow from South America

Archaeological Central American maize genomes suggest ancient gene flow from South America Logan Kistlera,1, Heather B. Thakarb, Amber M. VanDerwarkerc, Alejandra Domicd,e, Anders Bergströmf, Richard J. Georgec, Thomas K. Harperd, Robin G. Allabyg, Kenneth Hirthd, and Douglas J. Kennettc,1 aDepartment of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560; bDepartment of Anthropology, Texas A&M University, College Station, TX 77843; cDepartment of Anthropology, University of California, Santa Barbara, CA 93106; dDepartment of Anthropology, The Pennsylvania State University, University Park, PA 16802; eDepartment of Geosciences, The Pennsylvania State University, University Park, PA 16802; fAncient Genomics Laboratory, The Francis Crick Institute, NW1 1AT London, United Kingdom; and gSchool of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom Edited by David L. Lentz, University of Cincinnati, Cincinnati, OH, and accepted by Editorial Board Member Elsa M. Redmond November 3, 2020 (received for review July 24, 2020) Maize (Zea mays ssp. mays) domestication began in southwestern 16). However, precolonial backflow of divergent maize varieties Mexico ∼9,000 calendar years before present (cal. BP) and humans into Central and Mesoamerica during the last 9,000 y remains dispersed this important grain to South America by at least 7,000 understudied, and could have ramifications for the history of cal. BP as a partial domesticate. South America served as a second- maize as a staple in the region. ary improvement center where the domestication syndrome be- Morphological evidence from ancient maize found in ar- came fixed and new lineages emerged in parallel with similar chaeological sites combined with DNA data confirms a complex processes in Mesoamerica. Later, Indigenous cultivators carried a and extended domestication history. The earliest maize cobs second major wave of maize southward from Mesoamerica, but it found in the highlands of Oaxaca, Mexico dating to 6,250 cal. BP has been unclear until now whether the deeply divergent maize are small, and have two nondisarticulating vertical rows of al- lineages underwent any subsequent gene flow between these re- ternating seeds (17, 18) indicating that Indigenous cultivators gions. Here we report ancient maize genomes (2,300–1,900 cal. BP) were controlling plant reproduction. Early four-row cobs from from El Gigante rock shelter, Honduras, that are closely related to Mexico’s Tehuacán Valley (5,300-4,950 cal. BP) are also small, ancient and modern maize from South America. Our findings sug- and show comparable evidence for nondisarticulating seeds con- ANTHROPOLOGY gest that the second wave of maize brought into South America sistent with domestication (19, 20). Experimental work has shown hybridized with long-established landraces from the first wave, and that the lower atmospheric CO2 and temperatures in the Late that some of the resulting newly admixed lineages were then rein- Pleistocene and Early Holocene may have favored phenotypic troduced to Central America. Direct radiocarbon dates and cob mor- expression of maizelike inflorescence and seed architecture— phological data from the rock shelter suggest that more productive nonbranching stalk architecture and naked grains—which could maize varieties developed between 4,300 and 2,500 cal. BP. We hy- have been promoted and fixed by human-mediated selection (21, pothesize that the influx of maize from South America into Central 22). Ancient DNA data from Tehuacán cobs (San Marcos Cave) America may have been an important source of genetic diversity as dating between 5,300 and 4,950 cal. BP have alleles comparable to GENETICS maize was becoming a staple grain in Central and Mesoamerica. Significance maize | archaeogenomics | ancient DNA | agriculture | domestication Maize is a global food staple with great economic and cultural odern maize (Zea mays ssp. mays) is the world’smostpro- importance. Archaeogenomic studies have revealed a process Mductive staple crop (1) with over 1,100 million tons grown in of protracted maize domestication and multiple waves of 2018 (https://knoema.com/). Molecular data indicate that maize human-mediated dispersal in the Americas. Maize first arrived evolved from the annual grass teosinte (Zea mays ssp. parviglumus, in South America as a partial domesticate, where the domes- hereafter parviglumus) in southwestern Mexico, and that the first tication syndrome became independently fixed and improved steps toward domestication occurred ∼9,000 calendar years before varieties developed away from the influence of wild gene present (cal. BP) (2, 3). Starch grain and phytolith data from flow. We demonstrate that hybrids of some of these improved archeological sites in the Balsas region of southwestern Mexico varieties were likely reintroduced back to Central America. We confirm the early use of maize by ∼8,700 cal. BP (4). Archae- hypothesize that this backflow of South American genetic obotanical evidence also indicates dispersal of maize out of the material may have contributed to the development of a more Balsas through Central America by ∼7,500 cal. BP (5) and into productive staple, which was related to the growth and ag- South America by ∼7,000 cal. BP (6, 7) and ultimately into North gregation of human populations, and the formation of more America starting around 4,000 cal. BP (8). complex social and political structures regionally. Global dispersal of this productive crop beyond the Americas started with European contact with Native Americans in the 15th Author contributions: L.K. and D.J.K. designed research; L.K. performed research; L.K. and and 16th centuries (9). In addition to thousands of landraces K.H. contributed new reagents/analytic tools; L.K., H.B.T., A.M.V., A.D., A.B., R.J.G., T.K.H., – and R.G.A. analyzed data; L.K. and D.J.K. wrote the paper; and L.K., K.H., and D.J.K. developed by Indigenous cultivators in the Americas (10 15), ex- supervised research. perimentation worldwide has led to a staggering array of mor- The authors declare no competing interest. phological diversity and adaptations to a wide range of geographic This article is a PNAS Direct Submission. D.L.L. is a guest editor invited by the and climatic conditions. This diversity results from human- Editorial Board. mediated selection, reproductive isolation from parviglumus (and This open access article is distributed under Creative Commons Attribution-NonCommercial- related Zea mays ssp. mexicana, hereafter mexicana), secondary NoDerivatives License 4.0 (CC BY-NC-ND). improvement, and the potential reintroduction of new varieties 1To whom correspondence may be addressed. Email: [email protected] or kennett@anth. back to original homelands. A contemporary concern is the ucsb.edu. backflow of transgenic or commercial hybrid maize varieties to the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ Mexican heartland because gene flow with extant landraces can doi:10.1073/pnas.2015560117/-/DCSupplemental. result in the loss of genetic diversity and cultural knowledge (10, www.pnas.org/cgi/doi/10.1073/pnas.2015560117 PNAS Latest Articles | 1of6 Downloaded by guest on September 24, 2021 modern maize for inflorescence and seed architecture (td1 – tassel people lasting millennia between Central and South America. It is dwarf1; tb1 – teosinte branced1, ba1 – barren stalk1), circadian reasonable to suspect that maize, the most widespread crop spe- clock and flowering time (zmg1), and glycogen biosynthesis (bt2 – cies of the precolonial Americas, traveled back toward the do- brittle endosperm2) (23, 24). However, some alleles controlling mestication center in the hands of skilled farmers as part of this ear shattering and starch biosynthesis (zag1 – MADS-box gene; complex history. Here, we sequenced maize genomes from three su1 – sugary 1, and wx1 – waxy 1) were more teosintelike at that archaeological samples from El Gigante rock shelter in western point—four millennia after the onset of domestication. Intro- Honduras dating to between 2,300 and 1,900 cal. BP and compared gression with mexicana favored adaptation to drier and cooler these data to published modern landraces of maize and archaeo- conditions in the Mexican highlands, and most modern landraces logical samples from North, Central, and South America. We use from highland Mexico and Central America carry strong signals of these genomes as a temporal anchor to test the hypotheses that postdomestication mexicana admixture (13, 25). Continued in- humans moved maize from South America into Central America. In trogression within the natural range of parviglumus and mexicana this scenario, the reintroduced germplasm may have been impactful may also explain the gradual changes in cob size evident in the for the development of highly productive varieties. Isotopic evidence Tehuacán Valley (19). from Central America demonstrates substantial maize consumption The initial first wave of maize dispersal (7,500–7,000 cal. BP) as a staple grain beginning between4,700and4,000cal.BP(29). (5) through Central and South America likely occurred when Finally, we use morphological comparisons within the El Gigante maize was partially domesticated, and before the domestication maize assemblage to help constrain the timing of this gene flow. syndrome—the suite of characters setting a domesticated species apart from its wild counterpart—was fixed (26). Multiple waves El Gigante and Maize Samples

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