Evolution of Duplicate Control Regions in the Mitochondrial Genomes of Metazoa: A Case Study with Australasian Ixodes Ticks

Abstract

To investigate the evolution pattern and phylogenetic utility of duplicate control regions (CRs) in mitochondrial (mt) genomes, we sequenced the entire mt genomes of three Ixodes species and part of the mt genomes of another 11 species. All the species from the Australasian lineage have duplicate CRs, whereas the other species have one CR. Sequence analyses indicate that the two CRs of the Australasian Ixodes ticks have evolved in concert in each species. In addition to the Australasian Ixodes ticks, species from seven other lineages of metazoa also have mt genomes with duplicate CRs. Accumulated mtDNA sequence data from these metazoans and two recent experiments on replication of mt genomes in human cell lines with duplicate CRs allowed us to re-examine four intriguing questions about the presence of duplicate CRs in the mt genomes of metazoa: (1) Why do some mt genomes, but not others, have duplicate CRs? (2) How did mt genomes with duplicate CRs evolve? (3) How could the nucleotide sequences of duplicate CRs remain identical or very similar over evolutionary time? (4) Are duplicate CRs phylogenetic markers? It appears that mt genomes with duplicate CRs have a selective advantage in replication over mt genomes with one CR. Tandem duplication followed by deletion of genes is the most plausible mechanism for the generation of mt genomes with duplicate CRs. Once duplicate CRs occur in an mt genome, they tend to evolve in concert, probably by gene conversion. However, there are lineages where gene conversion may not always occur, and, thus, the two CRs may evolve independently in these lineages. Duplicate CRs have much potential as phylogenetic markers at low taxonomic levels, such as within genera, within families, or among families, but not at high taxonomic levels, such as among orders.

Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidae (albatrosses)

“…The duplicates include identical partial Cyt b sequences that lack an initiation codon and that are therefore functionless, even though nonfunctional copies are expected to degenerate and disappear rapidly under the tandem duplication and random loss model (Moritz and Brown, 1986;Boore, 2000). These findings suggest that gene conversions have occurred multiple times and maintained two identical or nearly identical copies, in accordance with previous studies (Abbott et al, 2005;Shao et al, 2005a). Although the duplicated content in the Cyt b sequence in Phoebastria is different from Thalassarche, the duplication might have originated in a common ancestor of the two genera.…”

“…Gene conversion also appears to occur in duplicated mtDNA sequences. This is based on observations of mtDNAs containing two identical or nearly identical copies that are shared with sister species, and which are more similar to each other than to the other copy in a different species (Shao et al, 2005a). Sequence duplications in the mt genome frequently involve the control region (CR), which is associated with the initiation of transcription and mtDNA replication.…”

“…Sequence duplications in the mt genome frequently involve the control region (CR), which is associated with the initiation of transcription and mtDNA replication. Duplicated and concertedly evolved CRs have been reported in snakes (Kumazawa et al, 1996(Kumazawa et al, , 1998, sea cucumbers (Arndt and Smith, 1998), ticks (Black and Roehrdanz, 1998;Campbell and Barker, 1999;Shao et al, 2005a), birds (Eberhard et al, 2001;Abbott et al, 2005;Jouventin et al, 2006;Gibb et al, 2007;Smith et al, 2007;Lawrence et al, 2008;Cho et al, 2009;Gomez-Diaz et al, 2009), fish (Lee et al, 2001;Tatarenkov and Avise, 2007), thrips (Shao et al, 2003), lizards (Kumazawa and Endo, 2004;Amer and Kumazawa, 2005), a sea firefly (Ogoh and Ohmiya, 2004), cephalopods (Yokobori et al, 2004), a frog (Sano et al, 2005), mites (Shao et al, 2005b(Shao et al, , 2006, and turtles (Parham et al, 2006a(Parham et al, , 2006b). Some of the duplications involve structural genes or tRNAs (Kumazawa et al, 1998;Campbell and Barker, 1999;Eberhard et al, 2001;Yokobori et al, 2004;Abbott et al, 2005;Shao et al, 2005b;Parham et al, 2006b;Gibb et al, 2007;Cho et al, 2009).…”

The mitochondrial genome of Conus textile, coxI–coxII intergenic sequences and Conoidean evolution

“…However, in birds duplication has been reported in which one of the copies of the CR is a degenerate control region. Shao et al (Shao et al, 2005) suggested that the two CRs may evolve independently and that duplicate CRs may be useful markers at the genus or family level.…”

Next-generation sequencing as means to retrieve tick systematic markers, with the focus on Nuttalliella namaqua (Ixodoidea: Nuttalliellidae)

“…In most cases several independent PCR amplification steps need to be performed and several clones need to be sequenced, making targeting of independent genes cumbersome and increasing the probability for sequencing errors. For tick systematics these basic approaches have been extensively used (Black and Piesman, 1994;Black et al 1997;Black and Roehrdanz, 1998;Klompen et al 2000;Shao et al 2004;Shao et al 2005;Klompen et al 2007). Next-generation sequencing has been used to sequence amplified nuclear and mitochondrial PCR products (Burger et al 2012;Burger et al 2013;Xiong et al 2013;Burger et al 2014).…”