Accommodating heterogenous rates of evolution in molecular divergence dating methods: an example using intercontinental dispersal of Plestiodon (Eumeces) lizards.

Identifying and dating historical biological events is a fundamental goal of evolutionary biology, and recent analytical advances permit the modeling of factors known to affect both the accuracy and the precision of molecular date estimates. As the use of multilocus data sets becomes increasingly routine, it becomes more important to evaluate the potentially confounding effects of rate heterogeneity both within (e.g., codon positions) and among loci when estimating divergence times. Here, using Plestiodon lizards as a test case, we examine the effects of accommodating rate heterogeneity among data partitions on divergence time estimation. Plestiodon inhabits both East Asia and North America, yet both the geographic origin of the genus and timing of dispersal between the continents have been debated. For each of the eight independently evolving loci and a combined data set, we conduct single model and partitioned analyses. We found that extreme saturation has obscured the underlying rate of evolution in the mitochondrial DNA (mtDNA), resulting in severe underestimation of the rate in this locus. As a result, the age of the crown Plestiodon clade was overestimated by 15-17 Myr by the unpartitioned analysis of the combined loci data. However, the application of partition-specific models to the combined data resulted in ages that were fully congruent with those inferred by the individual nuclear loci. Although partitioning improved divergence date estimates of the mtDNA-only analysis, the ages were nonetheless overestimated, thus indicating an inadequacy of our current models to capture the complex nature of mtDNA evolution in over large time scales. Finally, the statistically incongruent age distributions inferred by the partitioned and unpartitioned analyses of the combined data support mutually exclusive hypotheses of the timing of intercontinental dispersal of Plestiodon from Asia to North America. Analyses that best capture the rate of evolution in the combined data set infer that this exchange occurred via Beringia ∼18.0-30 Ma.

[1]  S. Manchester.  Biogeographical Relationships of North American Tertiary Floras , 1999 .

[2]  J. Huelsenbeck,et al.  Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. , 2004, Molecular biology and evolution.

[3]  J. Wen.  Evolution of Eastern Asian and Eastern North American Disjunct Distributions in Flowering Plants , 1999 .

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

[5]  J. Wiens,et al.  WHY DOES A TRAIT EVOLVE MULTIPLE TIMES WITHIN A CLADE? REPEATED EVOLUTION OF SNAKELIKE BODY FORM IN SQUAMATE REPTILES , 2006, Evolution; international journal of organic evolution.

[6]  Sylvia Richardson,et al.  Markov Chain Monte Carlo in Practice , 1997 .

[7]  H. Jeffreys.  Some Tests of Significance, Treated by the Theory of Probability , 1935, Mathematical Proceedings of the Cambridge Philosophical Society.

[8]  W. C. Culbertson,et al.  Strippable lignite Deposits, Slope and Bowman Counties, North Dakota , 1955 .

[9]  E. Louis,et al.  Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. , 2004, Systematic biology.

[10]  W. Berggren,et al.  Eocene-Oligocene Climatic and Biotic Evolution , 1992 .

[11]  B. MacFadden,et al.  Large temperature drop across the Eocene–Oligocene transition in central North America , 2007, Nature.

[12]  J. A. Wolfe.  Late Cretaceous-Cenozoic history of deciduousness and the terminal Cretaceous event , 1987, Paleobiology.

[13]  F. Ayala.  Molecular systematics , 2004, Journal of Molecular Evolution.

[14]  R. Murphy,et al.  A CLADISTIC EVALUATION OF THE COSMOPOLITAN GENUS Eumeces WIEGMANN (REPTILIA, SQUAMATA, SCINCIDAE) , 2011 .

[15]  F. K. Barker,et al.  The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. , 2006, Systematic biology.

[16]  F. Santini,et al.  The influence of model averaging on clade posteriors: an example using the triggerfishes (Family Balistidae). , 2008, Systematic biology.

[17]  S. Kelley,et al.  Rapid development of multiple nuclear loci for phylogenetic analysis using genomic resources: an example from squamate reptiles. , 2008, Molecular phylogenetics and evolution.

[18]  Walter R. Gilks,et al.  Hypothesis testing and model selection , 1995 .

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

[20]  D. Graur,et al.  Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. , 2004, Trends in genetics : TIG.

[21]  L. M. M.-T..  Theory of Probability , 1929, Nature.

[22]  B. Venkatesh,et al.  The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. , 2005, Gene.

[23]  A. Queiroz.  For Consensus (Sometimes) , 1993 .

[24]  W. Berggren,et al.  Toward a Revised Paleogene Geochronology , 1992 .

[25]  R. Estes.  Notes on Some Paleocene Lizards , 1965 .

[26]  O. Madsen,et al.  Molecular phylogeny and divergence times of Malagasy tenrecs: Influence of data partitioning and taxon sampling on dating analyses , 2008, BMC Evolutionary Biology.

[27]  Hirohisa Kishino,et al.  Divergence time and evolutionary rate estimation with multilocus data. , 2002, Systematic biology.

[28]  M. Schervish,et al.  Bayes Factors: What They are and What They are Not , 1999 .

[29]  F. Burbrink,et al.  How and when did Old World ratsnakes disperse into the New World? , 2007, Molecular phylogenetics and evolution.

[30]  M. Pagel,et al.  Bayesian estimation of ancestral character states on phylogenies. , 2004, Systematic biology.

[31]  J. A. Wolfe.  Distribution of major vegetational types during the Tertiary , 2013 .

[32]  Richard H. Ree,et al.  Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. , 2008, Systematic biology.

[33]  Ziheng Yang,et al.  Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. , 2006, Molecular biology and evolution.

[34]  D. Pearl,et al.  High-resolution species trees without concatenation , 2007, Proceedings of the National Academy of Sciences.

[35]  R. Cifelli,et al.  A new teiid lizard from the Cedar Mountain Formation (Albian–Cenomanian Boundary) of Utah , 2002 .

[36]  Chad D. Brock,et al.  DO REEFS DRIVE DIVERSIFICATION IN MARINE TELEOSTS? EVIDENCE FROM THE PUFFERFISH AND THEIR ALLIES (ORDER TETRAODONTIFORMES) , 2007, Evolution; international journal of organic evolution.

[37]  S. Evans,et al.  Early Cretaceous lizards from the Okurodani Formation of Japan , 1999 .

[38]  W. Maddison.  Gene Trees in Species Trees , 1997 .

[39]  J. Bull,et al.  Partitioning and combining data in phylogenetic analysis , 1993 .

[40]  K. Miller.  Middle Eocene to Oligocene stable isotopes, climate, and deep-water history : The terminal Eocene event? , 1992 .

[41]  H. Shaffer,et al.  Assessing Concordance of Fossil Calibration Points in Molecular Clock Studies: An Example Using Turtles , 2004, The American Naturalist.

[42]  Michael S. Y. Lee,et al.  Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. , 2007, Systematic biology.

[43]  L. Sloan,et al.  Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present , 2001, Science.

[44]  M. Miya,et al.  Unique patterns of pelvic fin evolution: a case study of balistoid fishes (Pisces: Tetraodontiformes) based on whole mitochondrial genome sequences. , 2009, Molecular phylogenetics and evolution.

[45]  Fredrik Ronquist,et al.  Patterns of animal dispersal, vicariance and diversification in the Holarctic , 2001 .

[46]  H. Philippe,et al.  A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. , 2004, Molecular biology and evolution.

[47]  Marc A Suchard,et al.  A nonparametric method for accommodating and testing across-site rate variation. , 2007, Systematic biology.

[48]  Adrian E. Raftery,et al.  Hypothesis testing and model selection , 1996 .

[49]  C. Denham,et al.  Magnetostratigraphy of the White River Group and its implications for oligocene geochronology , 1983 .

[50]  Alexei J. Drummond,et al.  Bayesian Phylogeography Finds Its Roots , 2009, PLoS Comput. Biol..

[51]  J. A. Wolfe.  Some Aspects of Plant Geography of the Northern Hemisphere During the Late Cretaceous and Tertiary , 1975 .

[52]  F. Sperling.  Molecular Systematics, 2nd ed. , 1997 .

[53]  James C. Wilgenbusch,et al.  AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics , 2008, Bioinform..

[54]  J. A. Wolfe.  A Paleobotanical Interpretation of Tertiary Climates in the Northern Hemisphere , 1978 .

[55]  M. Mckenna.  Holarctic Landmass Rearrangement, Cosmic Events, and Cenozoic Terrestrial Organisms , 1983 .

[56]  J. Inoue,et al.  The mitochondrial genome of spotted green pufferfish Tetraodon nigroviridis (Teleostei: Tetraodontiformes) and divergence time estimation among model organisms in fishes. , 2006, Genes & genetic systems.

[57]  A. Schmitz,et al.  Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. , 2005, Systematic biology.

[58]  S. Evans.  At the feet of the dinosaurs: the early history and radiation of lizards , 2003, Biological reviews of the Cambridge Philosophical Society.

[59]  C. M. Bogert,et al.  The systematic position of Lanthanotus and the affinities of the anguinomorphan lizards. Bulletin of the AMNH ; v. 105, article 1 , 2016 .

[60]  J. Conrad.  Phylogeny And Systematics Of Squamata (Reptilia) Based On Morphology , 2008 .

[61]  G. Schwarz.  Estimating the Dimension of a Model , 1978 .

[62]  S. Ho,et al.  Evidence for time dependency of molecular rate estimates. , 2007, Systematic biology.

[63]  P. Green.  Reversible jump Markov chain Monte Carlo computation and Bayesian model determination , 1995 .

[64]  A. Kluge.  A Concern for Evidence and a Phylogenetic Hypothesis of Relationships among Epicrates (Boidae, Serpentes) , 1989 .

[65]  M. Mckenna.  Cenozoic Paleogeography of North Atlantic Land Bridges , 1983 .

[66]  John J. Wiens,et al.  Weighting, Partitioning, and Combining Characters in Phylogenetic Analysis , 1994 .

[67]  S. Ho,et al.  Molecular clocks: when times are a-changin'. , 2006, Trends in genetics : TIG.

[68]  B. Rannala,et al.  Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. , 2004, Systematic biology.

[69]  D. Embert,et al.  MOLECULAR STUDIES ON THE GENUS EUMECES WIEGMANN, 1834: PHYLOGENETIC RELATIONSHIPS AND TAXONOMIC IMPLICATIONS , 2004 .

[70]  Jeremy M. Brown,et al.  The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. , 2007, Systematic biology.

[71]  Henk Brinkhuis,et al.  Climate Transition Global Cooling During the Eocene-Oligocene , 2009 .

[72]  E. H. Taylor,et al.  A Taxonomic Study of the Cosmopolitan Scincoid Lizards of the Genus Eumeces with an Account of the Distributional Relationships of Its Species , 1936 .

[73]  H. Lagarry,et al.  Depositional environments, lithostratigraphy, and biostratigraphy of the White River and Arikaree groups : late Eocene to early Miocene, North America , 1998 .

[74]  D. Wake,et al.  Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. , 2009, Molecular phylogenetics and evolution.

[75]  M. Phillips.  Branch-length estimation bias misleads molecular dating for a vertebrate mitochondrial phylogeny. , 2009, Gene.

[76]  B. Tiffney.  Perspectives on the origin of the floristic similarity between Eastern Asia and Eastern North America , 1985 .

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

[78]  Douglas L Altshuler,et al.  Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. , 2007, Systematic biology.

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

[80]  C. Janis.  Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events , 1993 .

[81]  B. Tiffney.  The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the northern hemisphere , 1985 .

[82]  M. Mckenna.  Fossil Mammals and Early Eocene North Atlantic Land Continuity , 1975 .

[83]  Shixia Xu,et al.  Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales , 2009, BMC Evolutionary Biology.

[84]  John R. Clark,et al.  A comparative study in ancestral range reconstruction methods: retracing the uncertain histories of insular lineages. , 2008, Systematic biology.