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

Abstract

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.

Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications

“…4A). This special phenomenon of mitogenomes with duplicate CRs, has also been observed in birds (Morris-Pocock et al, 2010;Schirtzinger et al, 2012), snakes (Kumazawa et al, 1996), sea cucumbers (Arndt and Smith, 1998), flatfishes (Li et al, 2015), sea firefly (Ogoh and Ohmiya, 2004) and ticks (Shao et al, 2005). However, the duplicated CRs identified in the present work are the first to be found in the Orthoptera.…”

The complete mitochondrial genome of Gammarus roeselii (Crustacea, Amphipoda): insights into mitogenome plasticity and evolution

“…As in G. roeselii, both Caprella species possess highly similar duplicated CR copies. Beyond amphipods, CR duplications have been observed in several animal species, including some species of ticks (Black & Roehrdanz, 1998;Campbell & Barker, 1999), ostracods (Ogoh & Ohmiya, 2004), sea cucumbers (Arndt & Smith, 1998), katydids (Yang et al, 2016), birds (Abbott et al, 2005;Morris-Pocock et al, 2010;Schirtzinger et al, 2012), turtles (Parham et al, 2006a, b;Peng et al, 2006), snakes (Kumazawa et al, 1996(Kumazawa et al, , 1998Dubey et al, 2012) and fishes (Lee et al, 2001;Tatarenkov & Avise, 2007;Shi et al, 2014). Sometimes, CR duplications extend beyond the sole CR, as exemplified by terrestrial isopods in which the entire mt genome is duplicated (Marcadé et al, 2007;Chandler et al, 2015;Peccoud et al, 2017).…”

Characterization of the complete mitochondrial genome of Cynoglossus gracilis and a comparative analysis with other Cynoglossinae fishes

“…Gene order in vertebrate mtDNA is thought to be quite conserved, especially in fishes (Clayton, 1992;Manchado et al, 2007). However, an increasing number of gene rearrangements in mtDNA have been identified in many taxa, including reptiles (Mueller and Boore, 2005;Okajima and Kumazawa, 2010), birds (Bensch and Harlid, 2000;Schirtzinger et al, 2012;Verkuil et al, 2010), amphibians (Macey et al, 1997;Sano et al, 2005), and fishes (Gong et al, 2013a;Inoue et al, 2003;Kong et al, 2009;Ki et al, 2008;Mabuchi et al, 2004;Ponce et al, 2008;Shi et al, 2013Shi et al, , 2014aShi et al, , 2015a.…”