A likelihood method for detecting trait-dependent shifts in the rate of molecular evolution.

Rate heterogeneity within groups of organisms is known to exist even when closely related taxa are examined. A wide variety of phylogenetic and dating methods have been developed that aim either to test for the existence of rate variation or to correct for its bias. However, none of the existing methods track the evolution of features that account for observed rate heterogeneity. Here, we present a likelihood model that assumes that rate variation is caused, in part, by species' intrinsic characteristics, such as a particular life-history trait, morphological feature, or habitat association. The model combines models of sequence and character state evolution such that rates of sequence change depend on the character state of a lineage at each point in time. We test, using simulations, the power and accuracy of the model to determine whether rates of molecular evolution depend on a particular character state and demonstrate its utility using an empirical example with halophilic and freshwater daphniids.

[1]  M. O. Dayhoff A model of evolutionary change in protein , 1978 .

[2]  J. Huelsenbeck,et al.  A compound poisson process for relaxing the molecular clock. , 2000, Genetics.

[3]  Peng Li,et al.  Relative-Rate Test for Nucleotide Substitutions between Two Lineages , 1992 .

[4]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

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

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

[7]  J. Felsenstein Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

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

[9]  W. Li,et al.  Evidence for higher rates of nucleotide substitution in rodents than in man. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[10]  H. Kishino,et al.  Dating of the human-ape splitting by a molecular clock of mitochondrial DNA , 2005, Journal of Molecular Evolution.

[11]  M. Pagel Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  A. Wilson,et al.  Generation time and genomic evolution in primates. , 1973, Science.

[13]  M. Lynch,et al.  Transitions to Asexuality Result in Excess Amino Acid Substitutions , 2006, Science.

[14]  M. Gouy,et al.  Sensitivity of the relative-rate test to taxonomic sampling. , 1998, Molecular biology and evolution.

[15]  J. Felsenstein Cases in which Parsimony or Compatibility Methods will be Positively Misleading , 1978 .

[16]  Jonathan P. Bollback,et al.  Stochastic mapping of morphological characters. , 2003, Systematic biology.

[17]  M. O. Dayhoff,et al.  Atlas of protein sequence and structure , 1965 .

[18]  H. Kishino,et al.  Estimation of Divergence Times from Molecular Sequence Data , 2005 .

[19]  J. Welch,et al.  There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Matthew D. Rasmussen,et al.  Accurate gene-tree reconstruction by learning gene- and species-specific substitution rates across multiple complete genomes. , 2007, Genome research.

[21]  Rasmus Nielsen,et al.  Mapping mutations on phylogenies , 2005 .

[22]  A. Rambaut,et al.  Determinants of rate variation in mammalian DNA sequence evolution , 1996, Journal of Molecular Evolution.

[23]  Derek J. Taylor,et al.  ACCELERATED MOLECULAR EVOLUTION IN HALOPHILIC CRUSTACEANS , 2002, Evolution; international journal of organic evolution.

[24]  N. Goldman,et al.  Comparison of models for nucleotide substitution used in maximum-likelihood phylogenetic estimation. , 1994, Molecular biology and evolution.

[25]  M. Sanderson Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. , 2002, Molecular biology and evolution.

[26]  S. Guindon,et al.  Bayesian estimation of divergence times from large sequence alignments. , 2010, Molecular biology and evolution.

[27]  C. Laird,et al.  Rate of Fixation of Nucleotide Substitutions in Evolution , 1969, Nature.

[28]  J. Felsenstein Phylogenies from molecular sequences: inference and reliability. , 1988, Annual review of genetics.

[29]  Simon Whelan,et al.  Statistical Methods in Molecular Evolution , 2005 .

[30]  J. Huelsenbeck,et al.  SUCCESS OF PHYLOGENETIC METHODS IN THE FOUR-TAXON CASE , 1993 .

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

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

[33]  Steven G. Johnson,et al.  CONTRASTING PATTERNS OF SYNONYMOUS AND NONSYNONYMOUS SEQUENCE EVOLUTION IN ASEXUAL AND SEXUAL FRESHWATER SNAIL LINEAGES , 2007, Evolution; international journal of organic evolution.

[34]  Lindell Bromham,et al.  Molecular dating when rates vary. , 2005, Trends in ecology & evolution.

[35]  C. Whittle,et al.  Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants. , 2002, Molecular biology and evolution.

[36]  Marc Robinson-Rechavi,et al.  RRTree: Relative-Rate Tests between groups of sequences on a phylogenetic tree , 2000, Bioinform..

[37]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

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

[39]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[40]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[41]  Sheldon M. Ross,et al.  Stochastic Processes , 2018, Gauge Integral Structures for Stochastic Calculus and Quantum Electrodynamics.

[42]  Andrew P. Martin,et al.  Body size, metabolic rate, generation time, and the molecular clock. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[43]  B Rannala,et al.  Accommodating phylogenetic uncertainty in evolutionary studies. , 2000, Science.

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

[45]  M. O. Dayhoff,et al.  22 A Model of Evolutionary Change in Proteins , 1978 .

[46]  Frank Rutschmann,et al.  Molecular dating of phylogenetic trees : A brief review of current methods that estimate divergence times , 2022 .

[47]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[48]  Simon Whelan,et al.  Distributions of statistics used for the comparison of models of sequence evolution in phylogenetics , 1999 .

[49]  B. Rannala,et al.  Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method. , 1997, Molecular biology and evolution.

[50]  M. Chase,et al.  Environmental energy and evolutionary rates in flowering plants , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  L. Bromham Why do species vary in their rate of molecular evolution? , 2009, Biology Letters.

[52]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[53]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[54]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .

[55]  P. Hebert,et al.  The systematics of Australian Daphnia and Daphniopsis (Crustacea: Cladocera): a shared phylogenetic history transformed by habitat-specific rates of evolution , 2006 .

[56]  P. Lewis A likelihood approach to estimating phylogeny from discrete morphological character data. , 2001, Systematic biology.

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

[58]  Timothy D. O'Connor,et al.  Genotype–phenotype associations: substitution models to detect evolutionary associations between phenotypic variables and genotypic evolutionary rate , 2009, Bioinform..

[59]  V. Bryson,et al.  Evolving Genes and Proteins. , 1965, Science.

[60]  Ziheng Yang,et al.  A heuristic rate smoothing procedure for maximum likelihood estimation of species divergence times , 2004 .