Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region

Abstract

Background: The mitochondrial genomes of snakes are characterized by an overall evolutionary rate that appears to be one of the most accelerated among vertebrates. They also possess other unusual features, including short tRNAs and other genes, and a duplicated control region that has been stably maintained since it originated more than 70 million years ago. Here, we provide a detailed analysis of evolutionary dynamics in snake mitochondrial genomes to better understand the basis of these extreme characteristics, and to explore the relationship between mitochondrial genome molecular evolution, genome architecture, and molecular function. We sequenced complete mitochondrial genomes from Slowinski's corn snake (Pantherophis slowinskii) and two cottonmouths (Agkistrodon piscivorus) to complement previously existing mitochondrial genomes, and to provide an improved comparative view of how genome architecture affects molecular evolution at contrasting levels of divergence.

The complete mitochondrial genome of the Sichuan hot-spring keel-back (Thermophis zhaoermii; Serpentes: Colubridae) and a mitogenomic phylogeny of the snakes

“…Mitochondrial genome sequences have been widely used in molecular phylogenetic analyses of snakes (Kumazawa et al 1998;Dong and Kumazawa 2005;Douglas et al 2006;Jiang et al 2007;Castoe et al 2008;Yan et al 2008) since the first complete mitochondrial DNA (mtDNA) sequence of Dinodon semicarinatus was reported in 1998 (Kumazawa et al 1998). Other than universal mtDNA structures, many unique phenomena were discovered in the mitochondrial genomes of snakes, such as the duplication of the control region and its adjacent area in alethinophidian snakes, length reduction of all genes (Kumazawa et al 1998;Dong and Kumazawa 2005;Jiang et al 2007;Yan et al 2008), and a burst of unique amino acids substitutions (Castoe et al 2008).…”

The complete mitochondrial DNA sequence and the phylogenetic position of Achalinus meiguensis (Reptilia: Squamata)

“…The typical vertebrate mitochondrial tRNAs do exactly conform to the canonical secondary structure (usually visualized as the cloverleaf structure), and consist of the acceptor stem (7 bp), the TΨC arm (5 bp), the anticodon arm (5 bp (iii) Control regions. Presently, all snakes studied except the scolecophidian snakes Leptotyphlops dulcis, Ramphotyphlops australis and Typhlops murius, have a duplicated control region (CR2) between NADH dehydrogenase subunit 1 (ND1) and subunit 2 (ND2), in addition to a control region (CR1) adjacent to the 5′-end of the 12s rRNA as it is in other vertebrates [6] . A. meiguensis mitochondrial genome also has two control regions of which lengths are 1062 and 1063 bp, respectively, about 12.4% of the complete sequence.…”

“…A pseudogene for tRNA Pro exists in the 5′ vicinity of control region II in some snakes' mtDNAs [2,4,6,23,24] , but it is not found in A. meiguensis. Comparing the snakes' sequences, we discovered that the pseudogene for tRNA Pro was only found in most of the Caenophidia, but not in the Scolecophidia, the Henophidia, and some primitive species of the Caenophidia.…”

“…Prior to analyses, the best-fit model of the nucleotide substitution under the nested likelihood ratio model and Akaike Information Criterion was selected by the program MODELTEST v. 3.7 [37] . Three independent iterations were run for 3×10 6 generations, and sampled every 100 generations, with the first 3×10 6 generations (10%) discarded as burn-in. Parameters were plotted against generations to check that convergence had been reached well before the post burn-in portion of the data.…”

“…Several studies showed that the gross structure of mitochondrial genome in snakes was similar to these of the other vertebrates, which was characterized as: double-stranded, circular DNAs of 16-18 kb, and encodes genes for 13 proteins, 2 rRNAs and 22 tRNAs, as well as having a major noncoding or control region that contains signals for replicating the heavy strand of mtDNA and for transcription [3] . Some unique characteristics in snake mtDNA complete sequences have been clarified previously, including duplicated control regions, a compact size, an elevated evolutionary rate and truncated tRNAs, and other shortened [1,[4][5][6] . Based on morphological studies, the genus Achalinus (Peters, 1869) was put under Xenodermatinae in Colubridae [7,8] .…”