Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome

Abstract

Background: Although the plastid genome is highly conserved across most angiosperms, multiple lineages have increased rates of structural rearrangement and nucleotide substitution. These lineages exhibit an excess of nonsynonymous substitutions (i.e., elevated dN/dS ratios) in similar subsets of plastid genes, suggesting that similar mechanisms may be leading to relaxed and/or positive selection on these genes. However, little is known regarding whether these mechanisms continue to shape sequence diversity at the intraspecific level.

Results: We examined patterns of interspecific divergence and intraspecific polymorphism in the plastid genome of Campanulastrum americanum, and across plastid genes found a significant correlation between dN/dS and pN/pS (i.e., the within-species equivalent of dN/dS). A number of genes including ycf1, ycf2, clpP, and ribosomal protein genes exhibited high dN/dS ratios. McDonald-Kreitman tests detected little evidence for positive selection acting on these genes, likely due to the presence of substantial intraspecific divergence.

Conclusions: These results suggest that mechanisms leading to increased nucleotide substitution rates in the plastid genome are continuing to act at the intraspecific level. Accelerated plastid genome evolution may increase the likelihood of intraspecific cytonuclear genetic incompatibilities, and thereby contribute to the early stages of the speciation process.

Figure 1

Sequence divergence (A) and polymorphism (B) for Campanulastrum americanum protein coding plastid genes. Sequence divergence and polymorphism as estimated by the number of substitutions per site in the terminal branch leading to C. americanum or within the species, respectively. Black and white bars indicate substitutions at synonymous and non-synonymous sites, respectively.

Figure 2

Trees for clpP intronic (A) and exonic (B) sequence. Trees with maximum likelihood branch length estimates using Arabidopsis thaliana as an outgroup.

Figure 3

Relationship between the dN/dS and pN/pS ratios for Campanulastrum americanum protein coding plastid genes. Genes or concatenations with less than three SNPs, including clpP, are not shown. The three points with both an elevated dN/dS and pN/pS ratio are labeled.

Figure 4

Intraspecific first-generation (F1) hybrid of Campanulastrum americanum showing variegation. This variegation is representative of what is found when crossing between populations with high levels of genetic divergence, such as the divergence between Virginia and remaining three populations used in this study.