The origins of maize were the topic of vigorous debate for nearly a century, but neither the current genetic model nor earlier archaeological models account for the totality of available data, and recent work has highlighted the potential contribution of a wild relative, Zea mays ssp. mexicana . Our population genetic analysis reveals that the origin of modern maize can be traced to an admixture between ancient maize and Zea mays ssp. mexicana in the highlands of Mexico some 4000 years after domestication began. We show that variation in admixture is a key component of maize diversity, both at individual loci and for additive genetic variation underlying agronomic traits. Our results clarify the origin of modern maize and raise new questions about the anthropogenic mechanisms underlying dispersal throughout the Americas.

Contents Summary 395 I. Introduction 395 II. The genetic basis of maize domestication 396 III. The tempo of maize domestication 401 IV. Genetic interactions and selection during maize domestication 401 V. Gene networks of maize domestication alleles 404 VI. Implications of gene interactions on evolution and selection 404 VII. Conclusions 405 Acknowledgements 405 References 405 Summary: Domestication is a tractable system for following evolutionary change. Under domestication, wild populations respond to shifting selective pressures, resulting in adaptation to the new ecological niche of cultivation. Owing to the important role of domesticated crops in human nutrition and agriculture, the ancestry and selection pressures transforming a wild plant into a domesticate have been extensively studied. InZea mays, morphological, genetic and genomic studies have elucidated how a wild plant, the teosinteZ. mayssubsp.parviglumis, was transformed into the domesticateZ. mayssubsp.mays. Five major morphological differences distinguish these two subspecies, and careful genetic dissection has pinpointed the molecular changes responsible for several of these traits. But maize domestication was a consequence of more than just five genes, and regions throughout the genome contribute. The impacts of these additional regions are contingent on genetic background, both the interactions between alleles of a single gene and among alleles of the multiple genes that modulate phenotypes. Key genetic interactions include dominance relationships, epistatic interactions and pleiotropic constraint, including how these variants are connected in gene networks. Here, we review the role of gene interactions in generating the dramatic phenotypic evolution seen in the transition from teosinte to maize.

Transposable elements (TEs) constitute the majority of flowering plant DNA, reflecting their tremendous success in subverting, avoiding, and surviving the defenses of their host genomes to ensure their selfish replication. More than 85% of the sequence of the maize genome can be ascribed to past transposition, providing a major contribution to the structure of the genome. Evidence from individual loci has informed our understanding of how transposition has shaped the genome, and a number of individual TE insertions have been causally linked to dramatic phenotypic changes. Genome-wide analyses in maize and other taxa have frequently represented TEs as a relatively homogeneous class of fragmentary relics of past transposition, obscuring their evolutionary history and interaction with their host genome. Using an updated annotation of structurally intact TEs in the maize reference genome, we investigate the family-level dynamics of TEs in maize. Integrating a variety of data, from descriptors of individual TEs like coding capacity, expression, and methylation, as well as similar features of the sequence they inserted into, we model the relationship between attributes of the genomic environment and the survival of TE copies and families. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences reveal a diversity of survival strategies of TE families. Together these generate a rich ecology of the genome, with each TE family representing the evolution of a distinct ecological niche. We conclude that while the impact of transposition is highly family- and context-dependent, a family-level understanding of the ecology of TEs in the genome can refine our ability to predict the role of TEs in generating genetic and phenotypic diversity.

Significance: One fundamental analysis needed to interpret genome assemblies is genome alignment. Yet, accurately aligning regulatory and transposon regions outside of genes remains challenging. We introduce Anchored Wavefront alignment (AnchorWave), which implements a genome duplication informed longest path algorithm to identify collinear regions and performs base pair–resolved, end-to-end alignment for collinear blocks using an efficient two-piece affine gap cost strategy. AnchorWave improves the alignment under a number of scenarios: genomes with high similarity, large genomes with high transposable element activity, genomes with many inversions, and alignments between species with deeper evolutionary divergence and different whole-genome duplication histories. Potential use cases include genome comparison for evolutionary analysis of nongenic sequences and population genetics of taxa with large, repeat-rich genomes.

The seasonal timing of seed germination determines a plant’s realized environmental niche, and is important for adaptation to climate. The timing of seasonal germination depends on patterns of seed dormancy release or induction by cold and interacts with flowering-time variation to construct different seasonal life histories. To characterize the genetic basis and climatic associations of natural variation in seed chilling responses and associated life-history syndromes, we selected 559 fully sequenced accessions of the model annual species Arabidopsis thaliana from across a wide climate range and scored each for seed germination across a range of 13 cold stratification treatments, as well as the timing of flowering and senescence. Germination strategies varied continuously along 2 major axes: 1) Overall germination fraction and 2) induction vs. release of dormancy by cold. Natural variation in seed responses to chilling was correlated with flowering time and senescence to create a range of seasonal life-history syndromes. Genome-wide association identified several loci associated with natural variation in seed chilling responses, including a known functional polymorphism in the self-binding domain of the candidate gene DOG1. A phylogeny of DOG1 haplotypes revealed ancient divergence of these functional variants associated with periods of Pleistocene climate change, and Gradient Forest analysis showed that allele turnover of candidate SNPs was significantly associated with climate gradients. These results provide evidence that A. thaliana ’s germination niche and correlated life-history syndromes are shaped by past climate cycles, as well as local adaptation to contemporary climate.