The Rice Paradox: Multiple Origins but Single Domestication in Asian Rice

Abstract

The origin of domesticated Asian rice (Oryza sativa) has been a contentious topic, with conflicting evidence for either single or multiple domestication of this key crop species. We examined the evolutionary history of domesticated rice by analyzing de novo assembled genomes from domesticated rice and its wild progenitors. Our results indicate multiple origins, where each domesticated rice subpopulation (japonica, indica, and aus) arose separately from progenitor O. rufipogon and/or O. nivara. Coalescence-based modeling of demographic parameters estimate that the first domesticated rice population to split off from O. rufipogon was O. sativa ssp. japonica, occurring at ∼13.1-24.1 ka, which is an order of magnitude older then the earliest archeological date of domestication. This date is consistent, however, with the expansion of O. rufipogon populations after the Last Glacial Maximum ∼18 ka and archeological evidence for early wild rice management in China. We also show that there is significant gene flow from japonica to both indica (∼17%) and aus (∼15%), which led to the transfer of domestication alleles from early-domesticated japonica to proto-indica and proto-aus populations. Our results provide support for a model in which different rice subspecies had separate origins, but that de novo domestication occurred only once, in O. sativa ssp. japonica, and introgressive hybridization from early japonica to proto-indica and proto-aus led to domesticated indica and aus rice.

Keywords: crop species; adaptation; gene flow; introgressive hybridization.

Fig. 1

Species phylogeny for the Asian rice complex. Oryza punctata genome was used for rooting the tree but omitted from figure due to its evolutionary distance. Scale bar length represents number of substitutions per site. All nodes had 100% bootstrap support and were thus omitted from labeling. The phylogenetic tree had a log-likelihood (lnL) of –8,171,522.67.

Fig. 2

G-PhoCS estimated demographic model of the Asian rice complex. Each internal node has a median mutation rate calibrated divergence time (T) estimate (ka) with its 95% Highest Posterior Density (HPD) in parenthesis. Only the 95% HPD is shown for each ancestral effective population size (N_e). Arrows indicate the migration band and direction of gene flow. Arrows are labeled with median and 95% HPD for the total migration rate estimates.

Fig. 3

Phylogenomic methods for examining species relationship and admixture. The methods involve a rooted four-taxon phylogeny, specifically with three species (P1, P2, and P3) and an outgroup (O). P1 and P2 are most closely related to each other while P3 is an in-group taxon that is equally distant to both P1 and P2. (A) Gene tree topology test. T1, T2, and T3 represent total number of genes supporting Topology 1, 2, and 3, respectively. In this hypothetical example, Topology 1 is assumed to be the major topology. (B) ABBA-BABA test. N_ABBA and N_BABA represent total number of sites with the “ABBA” and “BABA” conformation, respectively.