Repeated sequence homogenization between the control and pseudo‐control regions in the mitochondrial genomes of the subfamily Aquilinae

Abstract

In birds, the noncoding control region (CR) and its flanking genes are the only parts of the mitochondrial (mt) genome that have been modified by intragenomic rearrangements. In raptors, two noncoding regions are present: the CR has shifted to a new position with respect to the ''ancestral avian gene order,'' whereas the pseudo-control region (CCR) is located at the original genomic position of the CR. As possible mechanisms for this rearrangement, duplication and transposition have been considered. During characterization of the mt gene order in Bonelli's eagle Hieraaetus fasciatus, we detected intragenomic sequence similarity between the two regions supporting the duplication hypothesis. We performed intra-and intergenomic sequence comparisons in H. fasciatus and other falconiform species to trace the evolution of the noncoding mtDNA regions in Falconiformes. We identified sections displaying different levels of similarity between the CR and CCR. On the basis of phylogenetic analyses, we outline an evolutionary scenario of the underlying mutation events involving duplication and homogenization processes followed by sporadic deletions. Apparently, homogenization may easily occur if sufficient sequence similarity between the CR and CCR exists. Moreover, homogenization itself allows perpetuation of this continued equalization, unless this process is stopped by deletion. The Pandionidae and the Aquilinae seem to be the only two lineages of Falconiformes where homology between both regions is still detectable, whereas in other raptors no similarity was found so far. In these two lineages, the process of sequence degeneration may have slowed down by homogenization events retaining high sequence similarity at least in some sections.In contrast to the nuclear genome, where duplications and rearrangements are an important driving force of genome evolution, the mitochondrial (mt) genome of vertebrates has a more or less conserved structure. Nevertheless, modifications and rearrangements were detected in several groups of vertebrates. For example, the exchange of the positions of tRNA genes has been found in marsupials (Pääbo et al., '91),

The complete mitochondrial genome of Accipiter virgatus and evolutionary history of the pseudo-control regions in Falconiformes

“…The most plausible suggested model for the rearrangement involves duplication and homogenization processes, followed by multiple deletions (Bensch and H€ arlid, 2000;Gibb et al, 2007;Cadahía et al, 2009). Except the lineages of Pandionidae and Aquilinae (Gibb et al, 2007;Cadahía et al, 2009), the similarity between the duplicate control regions found in S. cheela (Circaetinae) also supporting the duplication hypothesis (Fig.…”

“…Our newest findings demonstrated that this novel gene order had multiple independent origins in Falconiformes (Fig. 4) instead of a single ancestral mutation event (Cadahía et al, 2009). Consequently, gene order in Falconiformes should not be used as phylogenetic markers.…”

“…According to previous studies (Roques et al, 2004;Cadahía et al, 2009), we identified previously described conserved sequence blocks in the CR of A. virgatus, Spilornis cheela, Micrastur gilvicollis, Aegypius monachus ( Supplementary Fig. S1).…”

“…Regarding raptors, or birds of prey, there has been some good progress in recent years. For example, the intra-genomic similarity between CR and CCR have been detected in two lineages of Falconiformes species (Pandionidae and Aquilinae), and tandem duplication followed by deletion of redundant copies of genes have been suggested the most plausible pattern for the generation of duplicate control regions in mt-genomes (Gibb et al, 2007;Cadahía et al, 2009). Further, the CCR has been used as a molecular marker for phylogenetic studies (V€ ali, 2002).…”

“…Moreover, several studies suggested the duplicate control regions could either evolve independently or evolve in concert (Arndt and Smith, 1998;Shao et al, 2005). In order to consist with earlier studies (Haring et al, 1999;V€ ali, 2002;Cadahía et al, 2009), we maintained to define the term CCR as the pseudo-control region located downstream of the functional CR.…”