The Genetic Architecture of the Maize Progenitor, Teosinte, and How It Was Altered During Maize Domestication

The genetics of domestication has been extensively studied ever since the rediscovery of Mendel's law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high F-ST) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is "missing" in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect. Author summary Although the genetics of trait differences between crops and their progenitors has been extensively studied, far less is known about the genetic architecture of trait variation in crop progenitors and how this architecture was altered during domestication. Here, we address this issue by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. Our results show that genetic architecture was reshaped during domestication in multiple ways. Maize has a greatly reduced number of QTL for domestication traits relative to teosinte and alleles at these QTL show greater dominance in maize. QTL alleles of large effect are present in both maize and teosinte, but more common in maize. We observed that regions of the genome that are strongly differentiated between teosinte and maize (high F-ST) explain less additive variation in maize than teosinte and that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of heritability is "missing" in the sense that it not associated with detectable QTL, which suggests that the raw material for domestication was largely composed of vast numbers of QTL of diminishingly small effects.