Concerted evolution of duplicated mitochondrial control regions in three related seabird species

Abstract

Background: Many population genetic and phylogenetic analyses of mitochondrial DNA (mtDNA) assume that mitochondrial genomes do not undergo recombination. Recently, concerted evolution of duplicated mitochondrial control regions has been documented in a range of taxa. Although the molecular mechanism that facilitates concerted evolution is unknown, all proposed mechanisms involve mtDNA recombination.

Results: Here, we document a duplication of a large region (cytochrome b, tRNAThr, tRNAPro, ND6, tRNAGlu and the control region) in the mitochondrial genome of three related seabird species. To investigate the evolution of duplicate control regions, we sequenced both control region copies (CR1 and CR2) from 21 brown (Sula leucogaster), 21 red-footed (S. sula) and 21 blue-footed boobies (S. nebouxii). Phylogenetic analysis suggested that the duplicated control regions are predominantly evolving in concert; however, approximately 51 base pairs at the 5' end of CR1 and CR2 exhibited a discordant phylogenetic signal and appeared to be evolving independently.

Conclusions: Both the structure of the duplicated region and the conflicting phylogenetic signals are remarkably similar to a pattern found in Thalassarche albatrosses, which are united with boobies in a large clade that includes all procellariiform and most pelecaniform seabirds. Therefore we suggest that concerted evolution of duplicated control regions either is taxonomically widespread within seabirds, or that it has evolved many times.

Figure 1

Location of PCR primers within the duplication region of the sulid mitochondrial genome. Schematic representation of the duplicated portion of the sulid mitochondrial genome, and approximate locations of PCR primers. L-strand primers are listed underneath the schematic, while H-strand primers are listed above. Gene abbreviations are as follows: cyt b = cytochrome b, ND6 = NADH dehydrogenase subunit 6, 12S = 12SrRNA, CR1 and CR2 = control region 1 and control region 2, Thr = tRNA-Threonine, Pro = tRNA-Proline, Glu = tRNA-Glutamic acid, Phe = tRNA-Phenylalanine. Grey areas correspond to long repetitive regions in Domain III of the control regions that could not be sequenced completely. All primer sequences are given in Table 2.

Figure 2

Maximum likelihood phylogenetic trees for the 3' end of CR1 and CR2 sequences. Unrooted maximum likelihood phylogenetic tree for the 3' end of CR1 and CR2 sequences from 21 brown, red-footed and blue footed boobies each. Nodal support of major clades is shown first for 100 maximum likelihood bootstrap pseudo-replicates and then for Bayesian posterior probability.

Figure 3

Maximum likelihood cladograms for the 3' end of CR1 and CR2 sequences. Unrooted maximum likelihood phylogenetic trees for the 3' end of CR1 and CR2 for (a) brown, (b) blue-footed, and (c) red-footed boobies (shown as cladograms to make support values easier to read).