Improved characterisation of among-lineage rate variation in cetacean mitogenomes using codon-partitioned relaxed clocks

Background and aims. There is extensive variation in substitution rates among metazoan mitochondrial genomes, including differences among lineages and among sites. Differences in substitution rates among lineages are routinely taken into account in molecular phylogenetic and dating analyses. However, this is rarely the case for differences in the lineage-specific patterns of rate variation among sites. Materials and methods. We analysed an alignment of 32 cetacean mitogenomes using a partitioned relaxed-clock approach, in which a separate relaxed-clock model was applied to each of the three codon positions of the protein-coding genes. Results. By comparing Bayes factors, we found overwhelming support for this model compared with a strict-clock model and less-complex models comprising fewer relaxed clocks. Our analyses reveal the presence of substantial rate heterogeneity among cetacean lineages, and that these patterns of variation differ between codon positions. However, we find no evidence of mitochondrial rate autocorrelation throughout the cetacean phylogeny. Conclusions. Our study confirms the feasibility of applying a partitioned relaxed-clock model to mitogenomic data, and suggests that molecular phylogenetic and dating analyses may be improved by the application of these models.

[1]  A. Vogler,et al.  Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. , 2010, Molecular biology and evolution.

[2]  Hirohisa Kishino,et al.  Estimating absolute rates of synonymous and nonsynonymous nucleotide substitution in order to characterize natural selection and date species divergences. , 2004, Molecular biology and evolution.

[3]  W. Bruno,et al.  Performance of a divergence time estimation method under a probabilistic model of rate evolution. , 2001, Molecular biology and evolution.

[4]  S. Ho,et al.  Accuracy of rate estimation using relaxed-clock models with a critical focus on the early metazoan radiation. , 2005, Molecular biology and evolution.

[5]  D. Bryant,et al.  A general comparison of relaxed molecular clock models. , 2007, Molecular biology and evolution.

[6]  Alexei J Drummond,et al.  Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. , 2005, Molecular biology and evolution.

[7]  C. Millar,et al.  High mitogenomic evolutionary rates and time dependency. , 2009, Trends in genetics : TIG.

[8]  H. Akaike.  A new look at the statistical model identification , 1974 .

[9]  Marc A. Suchard,et al.  Many-core algorithms for statistical phylogenetics , 2009, Bioinform..

[10]  M. McGowen,et al.  Divergence date estimation and a comprehensive molecular tree of extant cetaceans. , 2009, Molecular phylogenetics and evolution.

[11]  S. Ho,et al.  Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. , 2009, Systematic biology.

[12]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[13]  R. Nielsen,et al.  Radiation of Extant Cetaceans Driven by Restructuring of the Oceans , 2009, Systematic biology.

[14]  Alexei J Drummond,et al.  Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. , 2006, Molecular biology and evolution.

[15]  Sergei L. Kosakovsky Pond,et al.  HyPhy: hypothesis testing using phylogenies , 2005, Bioinform..

[16]  T. Ohta,et al.  On the constancy of the evolutionary rate of cistrons , 2005, Journal of Molecular Evolution.

[17]  S. Muse,et al.  A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. , 1994, Molecular biology and evolution.

[18]  Sergei L. Kosakovsky Pond,et al.  Synonymous Substitution Rates Predict HIV Disease Progression as a Result of Underlying Replication Dynamics , 2007, PLoS Comput. Biol..

[19]  M. Suchard,et al.  Bayesian selection of continuous-time Markov chain evolutionary models. , 2001, Molecular biology and evolution.

[20]  Ziheng Yang,et al.  Inferring speciation times under an episodic molecular clock. , 2007, Systematic biology.

[21]  J. García‐Moreno.  Is there a universal mtDNA clock for birds , 2004 .

[22]  M. Donoghue,et al.  Rates of Molecular Evolution Are Linked to Life History in Flowering Plants , 2008, Science.

[23]  Simon Y W Ho,et al.  An examination of phylogenetic models of substitution rate variation among lineages , 2009, Biology Letters.

[24]  H. Philippe,et al.  Heterotachy, an important process of protein evolution. , 2002, Molecular biology and evolution.

[25]  H. Kishino,et al.  Estimating the rate of evolution of the rate of molecular evolution. , 1998, Molecular biology and evolution.

[26]  C. Simon,et al.  Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA , 2006 .

[27]  Stéphane Aris-Brosou,et al.  Effects of models of rate evolution on estimation of divergence dates with special reference to the metazoan 18S ribosomal RNA phylogeny. , 2002, Systematic biology.

[28]  Michael J. Sanderson,et al.  A Nonparametric Approach to Estimating Divergence Times in the Absence of Rate Constancy , 1997 .

[29]  R. Lanfear,et al.  Metabolic rate does not calibrate the molecular clock , 2007, Proceedings of the National Academy of Sciences.

[30]  Phillip Endicott,et al.  A Bayesian evaluation of human mitochondrial substitution rates. , 2008, American journal of human genetics.

[31]  D. Mindell,et al.  Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages , 2008, BMC Biology.

[32]  Xiaoguang Yang.  Bayesian inference of cetacean phylogeny based on mitochondrial genomes , 2009, Biologia.

[33]  N. Galtier,et al.  Mitochondrial DNA as a marker of molecular diversity: a reappraisal , 2009, Molecular ecology.

[34]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[35]  G. Serio,et al.  A new method for calculating evolutionary substitution rates , 2005, Journal of Molecular Evolution.

[36]  S. Palumbi,et al.  Big and slow: phylogenetic estimates of molecular evolution in baleen whales (suborder mysticeti). , 2009, Molecular biology and evolution.

[37]  Nicolas Galtier,et al.  The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals , 2009, BMC Evolutionary Biology.

[38]  R. Zink,et al.  Mitochondrial DNA under siege in avian phylogeography , 2008, Molecular ecology.

[39]  Ziheng Yang.  Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods , 1994, Journal of Molecular Evolution.

[40]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[41]  C. Stringer,et al.  Evaluating the mitochondrial timescale of human evolution. , 2009, Trends in ecology & evolution.