Catalytic RNAs are often regarded as molecular fossils from the RNA World,
yet it is usually difficult to get more specific information about their ev
olution. Here we have investigated the coevolution of group II intron RNA s
tructures with their intron-encoded reverse transcriptases (RTs). Unlike gr
oup I introns, there has been no obvious reshuffling between intron RNA str
uctures and ORFs. Of the six classes of intron structures that encode ORFs,
three are conventional forms of group II A1, B1, and B2 secondary structur
es, whereas the remaining classes are bacterial, are possibly associated wi
th the most primitive ORFs, and have unusual features and hybrid features o
f group IIA and group IIB intron structures. Based on these data, we propos
e a new model for the evolution of group II introns, designated the retroel
ement ancestor hypothesis, which predicts that the major RNA structural for
ms of group II introns developed through coevolution with the intron-encode
d protein rather than as independent catalytic RNAs, and that most ORF-less
introns are derivatives of ORF-containing introns. The model is supported
by the distribution of ORF-containing and ORF-less introns, and by numerous
examples of ORF-less introns that contain ORF remnants.