Open Access Research article

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

Zhi J Jiang12, Todd A Castoe34, Christopher C Austin5, Frank T Burbrink16, Matthew D Herron37, Jimmy A McGuire58, Christopher L Parkinson3 and David D Pollock9*

Author Affiliations

1 Department of Biological Sciences, Biological Computation and Visualization Center, Louisiana State University, Baton Rouge, LA, USA

2 Computational Biology, Scripps Florida, Jupiter, FL, USA

3 Department of Biology, University of Central Florida, Orlando, FL, USA

4 Department of Biochemistry and Molecular Genetics, University of Colorado Health Sciences Center, Aurora, CO, USA

5 Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA

6 Department of Biology, City University of New York, Staten Island, USA

7 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA

8 Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, USA

9 Department of Biochemistry and Molecular Genetics, University of Colorado Health Sciences Center, Aurora, CO, USA

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BMC Evolutionary Biology 2007, 7:123  doi:10.1186/1471-2148-7-123

Published: 26 July 2007

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.

Results

We present a Bayesian genetic approach that suggests that the duplicated control region can function as an additional origin of heavy strand replication. The two control regions also appear to have different intra-specific versus inter-specific evolutionary dynamics that may be associated with complex modes of concerted evolution. We find that different genomic regions have experienced substantial accelerated evolution along early branches in snakes, with different genes having experienced dramatic accelerations along specific branches. Some of these accelerations appear to coincide with, or subsequent to, the shortening of various mitochondrial genes and the duplication of the control region and flanking tRNAs.

Conclusion

Fluctuations in the strength and pattern of selection during snake evolution have had widely varying gene-specific effects on substitution rates, and these rate accelerations may have been functionally related to unusual changes in genomic architecture. The among-lineage and among-gene variation in rate dynamics observed in snakes is the most extreme thus far observed in animal genomes, and provides an important study system for further evaluating the biochemical and physiological basis of evolutionary pressures in vertebrate mitochondria.