Long-term evolution of the Luteoviridae: time scale and mode of virus speciation

Abstract

Despite their importance as agents of emerging disease, the time scale and evolutionary processes that shape the appearance of new viral species are largely unknown. To address these issues, we analyzed intra- and interspecific evolutionary processes in the Luteoviridae family of plant RNA viruses. Using the coat protein gene of 12 members of the family, we determined their phylogenetic relationships, rates of nucleotide substitution, times to common ancestry, and patterns of speciation. An associated multigene analysis enabled us to infer the nature of selection pressures and the genomic distribution of recombination events. Although rates of evolutionary change and selection pressures varied among genes and species and were lower in some overlapping gene regions, all fell within the range of those seen in animal RNA viruses. Recombination breakpoints were commonly observed at gene boundaries but less so within genes. Our molecular clock analysis suggested that the origin of the currently circulating Luteoviridae species occurred within the last 4 millennia, with intraspecific genetic diversity arising within the last few hundred years. Speciation within the Luteoviridae may therefore be associated with the expansion of agricultural systems. Finally, our phylogenetic analysis suggested that viral speciation events tended to occur within the same plant host species and country of origin, as expected if speciation is largely sympatric, rather than allopatric, in nature.

FIG. 1.

Estimates of the rate of nucleotide substitution per site in the gene with the lowest number of sequences within each Luteoviridae species using the real (blue diamonds) and randomized (red squares) dates of isolation, with 95% HPD values shown. In each case, the gene used is shown in parentheses under the name of the species.

FIG. 2.

Maximum clade credibility phylogeny of the family Luteoviridae based on the CPov data set using 20 sequences per species and an empirical prior distribution on the substitution rate. Branch tip times reflect the times of viral sampling. The tree is automatically rooted through the use of a relaxed molecular clock, and the total depth of the tree is the TMRCA of the family Luteoviridae. Asterisks indicate nodes with posterior probabilities of ≥0.90. Horizontal blue bars denote 95% HPD intervals for the age of each node. Vertical black bars delimit sequence clusters for each virus genus and species.

FIG. 3.

Recombination breakpoints in the RdRp and CP genes of members of the family Luteoviridae. Black boxes indicate the positions of clusters of recombination breakpoints. RdRp1 (red) and RdRp2 (blue) correspond to ORF1 and -2 encoding the RdRp, CP (green) indicates the CP gene, and MP (yellow) indicates the MP gene. BP Num is the number of recombination breakpoints in a 200-nt window.