Diversification of Rice Yellow Mottle Virus and Related Viruses Spans the History of Agriculture from the Neolithic to the Present

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Abstract
The mechanisms of evolution of plant viruses are being unraveled, yet the timescale of their evolution remains an enigma. To address this critical issue, the divergence time of plant viruses at the intra- and inter-specific levels was assessed. The time of the most recent common ancestor (TMRCA) of Rice yellow mottle virus (RYMV; genus Sobemovirus) was calculated by a Bayesian coalescent analysis of the coat protein sequences of 253 isolates collected between 1966 and 2006 from all over Africa. It is inferred that RYMV diversified approximately 200 years ago in Africa, i.e., centuries after rice was domesticated or introduced, and decades before epidemics were reported. The divergence time of sobemoviruses and viruses of related genera was subsequently assessed using the age of RYMV under a relaxed molecular clock for calibration. The divergence time between sobemoviruses and related viruses was estimated to be approximately 9,000 years, that between sobemoviruses and poleroviruses approximately 5,000 years, and that among sobemoviruses approximately 3,000 years. The TMRCA of closely related pairs of sobemoviruses, poleroviruses, and luteoviruses was approximately 500 years, which is a measure of the time associated with plant virus speciation. It is concluded that the diversification of RYMV and related viruses has spanned the history of agriculture, from the Neolithic age to the present. The timescale of the evolution of plant viruses is an enigma, and even its order of magnitude is unknown. This critical issue is addressed here by calculating the age of plant viruses. An accurate estimate of the age of Rice yellow mottle virus (RYMV) was obtained by statistical analysis of a set of dated sequences. The age of RYMV provides a reliable calibration of related viruses, applying recently developed relaxed molecular clock models. It was found that RYMV diversified approximately 200 years ago, and that inter-specific diversification ranged from 500 years to 9,000 years. Altogether, plant virus diversification has spanned the history of agriculture from the Neolithic age to the present. This suggests that the Neolithic was a period of epidemiological transition for plant virus diseases, as already proposed for infectious human diseases. Intrinsically, it is for the same reason: increased contacts between hosts, pathogens, and vectors. This is consistent with the view that RNA viruses have a recent origin, and that humans have become the world's greatest evolutionary force.