The genetic architecture of teosinte catalyzed and constrained maize domestication

Authors: YANG, CHIN JIAN - University Of Wisconsin; SAMAYOA, LUIS FERNANDO - North Carolina State University; Bradbury, Peter; OLUKOLU, BODE - North Carolina State University; XUE, WEI - University Of Wisconsin; YORK, ALESSANDRA - University Of Wisconsin; TUHOLSKI, MICHAEL - University Of Wisconsin; WANG, WEIDONG - University Of Wisconsin; DASKALSKA, LORA - University Of Wisconsin; NEUMEYER, MICHAEL - University Of Wisconsin; SANCHEZ-GONZALES, JOSE DE JESUS - University Of Guadalajara; ROMAY, MARIA - Cornell University; GLAUBITZ, JEFFREY - Cornell University; SUN, QI - Cornell University; Buckler, Edward - Ed; Holland, Jim - Jim; DOEBLEY, JOHN - University Of Wisconsin

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/12/2019
Publication Date: 3/4/2019
Citation: Yang, C., Samayoa, L., Bradbury, P., Olukolu, B.A., Xue, W., York, A.M., Tuholski, M.R., Wang, W., Daskalska, L.L., Neumeyer, M.A., Sanchez-Gonzales, J., Romay, M.C., Glaubitz, J.C., Sun, Q., Buckler IV, E.S., Holland, J.B., Doebley, J.F. 2019. The genetic architecture of teosinte catalyzed and constrained maize domestication. Proceedings of the National Academy of Sciences. 116:5643-5652.

Interpretive Summary: Maize was domesticated about 9000 years ago from teosinte, a wild grass native to Mexico. Teosinte still exists in many of the corn growing areas of Mexico. Landrace maize populations are like heirloom corn populations, they have been maintained by farmers over hundreds, perhaps thousands, of years. We wondered about the genetic variation that exists within maize landraces and how that might be related to genetic variation that exists in their wild relative, teosinte, growing in similar conditions. Natural selection shapes the variability that exists in natural populations like teosinte, whereas a combination of natural selection and human selection for specific characteristics (typically ear and kernel appearance) as well as general productivity impacts the variation in domesticated populations. We compared a teosinte and landrace population sampled from the same town in Mexico for heritable variation and genetic correlations for a large number of traits. We found that maize has less heritable variation than teosinte, probably because human selection during domestication reduced the genetic variation in maize. The pattern of trait correlations also shifted in maize compared to teosinte, as the restructuring of the maize ear lead to new developmental constraints. Finally, we found that almost all measured traits changed significantly on average between teosinte and maize, except total seed mass produced per plant. Landrace maize plants do not produce more ‘yield’ per plant than teosinte, unless perhaps they are grown at higher population density.

Technical Abstract: The process of evolution under domestication has been studied using phylogenetics, population genetics-genomics, QTL mapping, gene expression assays, and archaeology. Here we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. Curiously, we observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication are weak for all traits with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, non-neutral divergence between teosinte and maize landrace genetic variance-covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.