Artificial selection in domestication and breeding prevents speciation in rice

Abstract Speciation has long been regarded as an irreversible process once the reproductive barriers had been established. However, unlike in natural populations, artificial selection might either accelerate or prevent speciation processes in domesticated species. Asian cultivated rice is a target crop for both domestication and artificial breeding; it contains two subspecies of indica and japonica, which usually produce sterile inter-subspecific hybrids due to reproductive barriers. Here we constructed the evolutionary trajectory of a reproductive isolation system S5, which regulates fertility in indica-japonica hybrids via three adjacent genes, based on data of 606 accessions including two cultivated and 11 wild rice species. Although hybrid sterility haplotypes at S5 led to establishment of a killer-protector reproductive barrier, origin of wide-compatibility haplotypes by complex hybridization and recombination provided an opposing force to reproductive isolation and thus prevented speciation during domestication. Analysis in a diallel set of 209 crosses involving 21 parents showed that the wide-compatibility genotypes largely reduced sterility of indica-japonica hybrids indicating that wide compatibility gene would enable gene flow to maintain species coherence. This counter-acting system indicates that combined effects of natural evolution and artificial selection may result in reversible processes of speciation in rice, which may also have implications for rice genetic improvement.