Weedy rice (Oryza spp.) is a problematic weed of cultivated rice (O. sativa) around the world. Recent studies have established multiple independent evolutionary origins of weedy rice, raising questions about the traits and genes that are essential for the evolution of this weed. Among world regions, South Asia stands out due to the heterogeneity of its weedy rice populations, which can be traced to at least three origins: two through de-domestication from distinct cultivated rice varieties, and one from local wild rice (O. rufipogon/O. nivara). Here we examine five traits considered typical of or advantageous to weedy rice in weedy, cultivated and wild rice samples from South Asia. We establish that convergence among all three weed groups occurs for easy seed shattering, red pericarp color, and compact plant architecture, suggesting that these traits are essential for weed success in the South Asian agricultural environment. A high degree of convergence for black hull color is also seen among weeds with wild ancestors and weeds evolved from the aus cultivated rice group. We also examine polymorphism in five known domestication candidate genes, and find that Rc and Bh4 are associated with weed seed pericarp color and hull color, respectively, and weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy-linked gene Sdr4. The presence of a domestication related allele at the seed shattering locus, sh4, in weedy rice populations with cultivated ancestry supports a de-domestication origin for these weedy groups, and raises questions about the reacquisition of the shattering trait in these weedy populations. Our characterization of weedy rice phenotypes in South Asia and their associated candidate genes contribute to the emerging understanding of the mechanisms by which weedy rice evolves worldwide, suggesting that standing ancestral variation is often the source of weedy traits in independently evolved groups, and highlighting the reservoir of genetic variation that is present in cultivated varieties as well as in wild rice, and its potential for phenotypic evolution.

Weedy rice (Oryza spp.) has successfully adapted to invasion of cultivated rice (O. sativa L.) fields by being a strong competitor from the early vegetative growth stages to crop harvest. While seed shattering and seed dormancy have been shown to contribute to competitiveness at the reproductive stage, much less is known about the traits that could contribute to weedy rice adaptation at the vegetative stage. We examined several growth and physiological traits in five different weedy rice lineages with different ancestral origins, and found that no single vegetative phenotype characterizes all weedy rice. Divergence in growth and physiological traits between weedy rice groups and their putative cultivated ancestors has been limited, suggesting that altered vegetative traits have not been a common path to weed adaptation. There is a lack of convergence in patterns of gene expression in two independent weedy rice lineages, suggesting that there are few shared genetic mechanisms in the evolution of vegetative traits. We conclude that it must not be assumed that all weedy rice groups necessarily have altered vegetative growth or physiological mechanisms compared to their ancestors, that facilitate their invasion of crop fields.