Pioneering archaeological expeditions lead by Richard MacNeish in the 1960s identified the valley of Tehuacán as an important center of early Mesoamerican agriculture, providing by far the widest collection of ancient crop remains, including maize. In 2012, a new exploration of San Marcos cave (Tehuacán, Mexico) yielded nonmanipulated maize specimens dating at a similar age of 5,300-4,970 calibrated y B.P. On the basis of shotgun sequencing and genomic comparisons to Balsas teosinte and modern maize, we show herein that the earliest maize from San Marcos cave was a partial domesticate diverging from the landraces and containing ancestral allelic variants that are absent from extant maize populations. Whereas some domestication loci, such as teosinte branched1 (tb1) and brittle endosperm2 (bt2), had already lost most of the nucleotide variability present in Balsas teosinte, others, such as teosinte glume architecture1 (tga1) and sugary1 (su1), conserved partial levels of nucleotide variability that are absent from extant maize. Genetic comparisons among three temporally convergent samples revealed that they were homozygous and identical by descent across their genome. Our results indicate that the earliest maize from San Marcos was already inbred, opening the possibility for Tehuacán maize cultivation evolving from reduced founder populations of isolated and perhaps self-pollinated individuals.maize | paleogenomics | teosinte | domestication | Tehuacán
Despite its global importance as a crop with broad economic, dietary, and cultural importance, the origins of maize and its closest wild relatives remained the topic of vigorous debate for nearly a century. Molecular analyses ultimately concluded that maize was domesticated once from a common ancestor with its closest extant relative, the lowland wild grass Zea mays ssp. parviglumis. But neither the current genetic model nor earlier models based on archaeological data account for the totality of available data, and recent work has highlighted the potential contribution of a second wild relative, the highland Zea mays ssp. mexicana. Here we present a detailed population genetic analysis of the contributions of both wild taxa to modern maize diversity using the largest sample of traditional maize varieties sequenced to date. We show that all modern maize can trace its origin to an ancient admixture event between domesticated ancient maize and Zea mays ssp. mexicana in the highlands of Mexico ca 5300 cal BP, some 4,000 years after domestication began. We show that variation in admixture is a key component of modern maize genetic and phenotypic diversity, both at the level of individual loci and as a factor driving a substantial component of additive genetic variation across a number of agronomic traits. Our results clarify the long-debated origin of modern maize, highlight the potential contributions of crop wild relatives to agronomic improvement, and raise new questions about the anthropogenic mechanisms underlying multiple waves of dispersal throughout the Americas.
The story of how preColumbian civilizations developed goes hand-in-hand with the process of plant domestication by Mesoamerican inhabitants. Here, we present the almost complete sequence of a mitochondrial genome and a partial chloroplast genome from an archaeological maize sample collected at the Valley of Tehuacán, México. Accelerator mass spectrometry dated the maize sample to be 5,040–5,300 years before present (95% probability). Phylogenetic analysis of the mitochondrial genome shows that the archaeological sample branches basal to the other Zea mays genomes, as expected. However, this analysis also indicates that fertile genotype NB is closely related to the archaeological maize sample and evolved before cytoplasmic male sterility genotypes (CMS-S, CMS-T, and CMS-C), thus contradicting previous phylogenetic analysis of mitochondrial genomes from maize. We show that maximum-likelihood infers a tree where CMS genotypes branch at the base of the tree when including sites that have a relative fast rate of evolution thus suggesting long-branch attraction. We also show that Bayesian analysis infer a topology where NB and the archaeological maize sample are at the base of the tree even when including faster sites. We therefore suggest that previous trees suffered from long-branch attraction. We also show that the phylogenetic analysis of the ancient chloroplast is congruent with genotype NB to be more closely related to the archaeological maize sample. As shown here, the inclusion of ancient genomes on phylogenetic trees greatly improves our understanding of the domestication process of maize, one of the most important crops worldwide.
Significance Despite their importance in supplying nutrients, root traits related to maize domestication are scarce. We used laser ablation tomography to characterize the root architecture and anatomy of 5,300-y-old maize specimens recovered from San Marcos (Tehuacán, Mexico), revealing exquisite preservation of their cellular organization. Outer cortical cells contained thick and lignified walls typical of extant maize adapted to hard soils. By contrast, the absence of seminal roots is only found in the maize ancestor, teosinte. Two genes important for seminal root development had mutations that could relate to their absence. Our results indicate that some traits related to drought adaptation were not fully present in the earliest maize from Tehuacán, providing clues to conditions prevailing during early maize cultivation.
A large collection of maize macro-specimens has been gathered from archaeological sites across the American continent, but only a few have been directly dated by accelerator mass spectrometry (AMS). We recently conducted two new excavations in several rock shelters of Tehuacán valley (San Marcos, Coxcatlán, and Purrón) and uncovered 132 non-manipulated macro-specimens of maize suitable for morphological and paleogenomic analysis, including many complete cobs, stalks, internodes, and leaves. Direct AMS dates for 43 samples found in San Marcos or Coxcatlán confirm the previously reported chronologies for these sites. By contrast, a cob found in Purrón was dated to 3060±30 before present (3360–3180 cal BP) (2σ), demonstrating that maize was present at that site at least 1500 calendar years earlier than previously expected, and suggesting that other specimens of similar age are still likely to be found in the southeastern region of the Tehuacán valley. A global comparison of macro-specimen chronology across the continent shows that the current archaebotanical record does not yet reflect the chronology of dispersal from central Mexico to northern or southern regions, opening the possibility for finding the missing links in subsequent expeditions within Mexico and Central America.
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