Multiple independent origins of mitochondrial control region duplications in the order Psittaciformes

Mitochondrial genomes are generally thought to be under selection for compactness, due to their small size, consistent gene content, and a lack of introns or intergenic spacers. As more animal mitochondrial genomes are fully sequenced, rearrangements and partial duplications are being identified with increasing frequency, particularly in birds (Class Aves). In this study, we investigate the evolutionary history of mitochondrial control region states within the avian order Psittaciformes (parrots and cockatoos). To this aim, we reconstructed a comprehensive multi-locus phylogeny of parrots, used PCR of three diagnostic fragments to classify the mitochondrial control region state as single or duplicated, and mapped these states onto the phylogeny. We further sequenced 44 selected species to validate these inferences of control region state. Ancestral state reconstruction using a range of weighting schemes identified six independent origins of mitochondrial control region duplications within Psittaciformes. Analysis of sequence data showed that varying levels of mitochondrial gene and tRNA homology and degradation were present within a given clade exhibiting duplications. Levels of divergence between control regions within an individual varied from 0-10.9% with the differences occurring mainly between 51 and 225 nucleotides 3′ of the goose hairpin in domain I. Further investigations into the fates of duplicated mitochondrial genes, the potential costs and benefits of having a second control region, and the complex relationship between evolutionary rates, selection, and time since duplication are needed to fully explain these patterns in the mitochondrial genome.

Graphical abstractDownload full-size imageHighlights► Of 117 parrot species surveyed 76 had a single control region, 38 had a duplicated control region, and three were unscorable. ► Six independent origins for control region duplications within the Psittaciformes were identified. ► Differences between the duplicated control regions within an individual ranged from 0-10.9%. ► All but two species with duplicated control regions had the gene order described by Eberhard et al. (2001) for Amazona parrots. ► Two Neotropical species retained a potentially functional tRNAPro in the duplicated section.