Episodic Evolution and Adaptation of Chloroplast Genomes in Ancestral Grasses

Background: It has been suggested that the chloroplast genomes of the grass family, Poaceae, have undergone an elevated evolutionary rate compared to most other angiosperms, yet the details of this phenomenon have remained obscure. To know how the rate change occurred during evolution, estimation of the time-scale with reliable calibrations is needed. The recent finding of 65 Ma grass phytoliths in Cretaceous dinosaur coprolites places the diversification of the grasses to the Cretaceous period, and provides a reliable calibration in studying the tempo and mode of grass chloroplast evolution. Methodology/Principal Findings: By using chloroplast genome data from angiosperms and by taking account of new paleontological evidence, we now show that episodic rate acceleration both in terms of non-synonymous and synonymous substitutions occurred in the common ancestral branch of the core Poaceae (a group formed by rice, wheat, maize, and their allies) accompanied by adaptive evolution in several chloroplast proteins, while the rate reverted to the slow rate typical of most monocot species in the terminal branches. Conclusions/Significance: Our finding of episodic rate acceleration in the ancestral grasses accompanied by adaptive molecular evolution has a profound bearing on the evolution of grasses, which form a highly successful group of plants. The widely used model for estimating divergence times was based on the assumption of correlated rates between ancestral and descendant lineages. However, the assumption is proved to be inadequate in approximating the episodic rate acceleration in the ancestral grasses, and the assumption of independent rates is more appropriate. This finding has implications for studies of molecular evolutionary rates and time-scale of evolution in other groups of organisms.