Shedding light on the ‘dark side’ of phylogenetic comparative methods

Summary Phylogenetic comparative methods are becoming increasingly popular for investigating evolutionary patterns and processes. However, these methods are not infallible – they suffer from biases and make assumptions like all other statistical methods. Unfortunately, although these limitations are generally well known in the phylogenetic comparative methods community, they are often inadequately assessed in empirical studies leading to misinterpreted results and poor model fits. Here, we explore reasons for the communication gap dividing those developing new methods and those using them. We suggest that some important pieces of information are missing from the literature and that others are difficult to extract from long, technical papers. We also highlight problems with users jumping straight into software implementations of methods (e.g. in r) that may lack documentation on biases and assumptions that are mentioned in the original papers. To help solve these problems, we make a number of suggestions including providing blog posts or videos to explain new methods in less technical terms, encouraging reproducibility and code sharing, making wiki‐style pages summarising the literature on popular methods, more careful consideration and testing of whether a method is appropriate for a given question/data set, increased collaboration, and a shift from publishing purely novel methods to publishing improvements to existing methods and ways of detecting biases or testing model fit. Many of these points are applicable across methods in ecology and evolution, not just phylogenetic comparative methods.

[1]  John-Arvid Grytnes,et al.  Niche conservatism as an emerging principle in ecology and conservation biology. , 2010, Ecology letters.

[2]  R. FitzJohn,et al.  The unsolved challenge to phylogenetic correlation tests for categorical characters. , 2015, Systematic biology.

[3]  Richard G FitzJohn,et al.  Model Adequacy and the Macroevolution of Angiosperm Functional Traits , 2014, bioRxiv.

[4]  Michelle R. Leishman,et al.  On misinterpreting the phylogenetic correction , 1995 .

[5]  Gavin H. Thomas,et al.  MOTMOT: models of trait macroevolution on trees , 2012 .

[6]  B. O’Meara Evolutionary Inferences from Phylogenies: A Review of Methods , 2012 .

[7]  T. F. Hansen,et al.  Phylogenies and the Comparative Method: A General Approach to Incorporating Phylogenetic Information into the Analysis of Interspecific Data , 1997, The American Naturalist.

[8]  Kate E. Jones,et al.  An optimum body size for mammals? Comparative evidence from bats , 1997 .

[9]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[10]  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.

[11]  Richard G FitzJohn,et al.  Quantitative traits and diversification. , 2010, Systematic biology.

[12]  G. Slater Correction to ‘Phylogenetic evidence for a shift in the mode of mammalian body size evolution at the Cretaceous–Palaeogene boundary’, and a note on fitting macroevolutionary models to comparative paleontological data sets , 2014 .

[13]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[14]  Peter E Midford,et al.  Estimating a binary character's effect on speciation and extinction. , 2007, Systematic biology.

[15]  A. King,et al.  Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution , 2004, The American Naturalist.

[16]  R. Freckleton Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence , 2000 .

[17]  Matthew W. Pennell,et al.  An integrative view of phylogenetic comparative methods: connections to population genetics, community ecology, and paleobiology , 2013, Annals of the New York Academy of Sciences.

[18]  N. Cooper,et al.  Body Size Evolution in Mammals: Complexity in Tempo and Mode , 2010, The American Naturalist.

[19]  R. A. Pyron,et al.  Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. , 2014, Ecology letters.

[20]  Lam Si Tung Ho,et al.  Asymptotic theory with hierarchical autocorrelation: Ornstein–Uhlenbeck tree models , 2013, 1306.1322.

[21]  Anthony R. Ives,et al.  Using the Past to Predict the Present: Confidence Intervals for Regression Equations in Phylogenetic Comparative Methods , 2000, The American Naturalist.

[22]  Liam J. Revell,et al.  phytools: an R package for phylogenetic comparative biology (and other things) , 2012 .

[23]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[24]  D. Rabosky,et al.  A Robust Semi-Parametric Test for Detecting Trait-Dependent Diversification. , 2016, Systematic biology.

[25]  Carl Boettiger,et al.  IS YOUR PHYLOGENY INFORMATIVE? MEASURING THE POWER OF COMPARATIVE METHODS , 2011, Evolution; international journal of organic evolution.

[26]  B. O’Meara,et al.  MODELING STABILIZING SELECTION: EXPANDING THE ORNSTEIN–UHLENBECK MODEL OF ADAPTIVE EVOLUTION , 2012, Evolution; international journal of organic evolution.

[27]  T. F. Hansen,et al.  Interpreting the evolutionary regression: the interplay between observational and biological errors in phylogenetic comparative studies. , 2012, Systematic biology.

[28]  Boris Igić,et al.  Species Selection Maintains Self-Incompatibility , 2010, Science.

[29]  Matthew W. Pennell,et al.  How much of the world is woody? , 2014 .

[30]  J. Losos,et al.  Seeing the Forest for the Trees: The Limitations of Phylogenies in Comparative Biology , 2011, The American Naturalist.

[31]  N. Cooper,et al.  Macroecology and extinction risk correlates of frogs , 2008 .

[32]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[33]  R M May,et al.  Extinction rates can be estimated from molecular phylogenies. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  F J Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[35]  T. F. Hansen,et al.  TRANSLATING BETWEEN MICROEVOLUTIONARY PROCESS AND MACROEVOLUTIONARY PATTERNS: THE CORRELATION STRUCTURE OF INTERSPECIFIC DATA , 1996, Evolution; international journal of organic evolution.

[36]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[37]  P. Harvey,et al.  Mammal life‐history evolution: a comparative test of Charnov's model , 1995 .

[38]  T. Garland,et al.  Phylogenetic logistic regression for binary dependent variables. , 2010, Systematic biology.

[39]  J. Felsenstein Maximum-likelihood estimation of evolutionary trees from continuous characters. , 1973, American journal of human genetics.

[40]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  D. Rabosky,et al.  Model inadequacy and mistaken inferences of trait-dependent speciation. , 2014, Systematic biology.

[42]  F James Rohlf A comment on phylogenetic correction. , 2006, Evolution; international journal of organic evolution.

[43]  T. F. Hansen STABILIZING SELECTION AND THE COMPARATIVE ANALYSIS OF ADAPTATION , 1997, Evolution; international journal of organic evolution.

[44]  James G. Lefevre,et al.  Independent contrasts and PGLS regression estimators are equivalent. , 2012, Systematic biology.

[45]  Thomas F Hansen,et al.  ASSESSING CURRENT ADAPTATION AND PHYLOGENETIC INERTIA AS EXPLANATIONS OF TRAIT EVOLUTION:THE NEED FOR CONTROLLED COMPARISONS , 2005, Evolution; international journal of organic evolution.

[46]  L. Cavalli-Sforza,et al.  PHYLOGENETIC ANALYSIS: MODELS AND ESTIMATION PROCEDURES , 1967, Evolution; international journal of organic evolution.

[47]  Yihui Xie,et al.  A General-Purpose Package for Dynamic Report Generation in R , 2016 .

[48]  R M May,et al.  The reconstructed evolutionary process. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  Lam Si Tung Ho,et al.  Intrinsic inference difficulties for trait evolution with Ornstein‐Uhlenbeck models , 2014 .

[50]  C. Osborne,et al.  Anatomical enablers and the evolution of C4 photosynthesis in grasses , 2012, Proceedings of the National Academy of Sciences.

[51]  Barbara R. Holland,et al.  Analysis of Phylogenetics and Evolution with R , 2007 .

[52]  Carl Boettiger,et al.  Is your phylogeny informative , 2012 .

[53]  R. Freckleton,et al.  A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies , 2015, Biological journal of the Linnean Society. Linnean Society of London.

[54]  F. James Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[55]  Andrew D Higginson,et al.  Heavy use of equations impedes communication among biologists , 2012, Proceedings of the National Academy of Sciences.

[56]  Robert P Freckleton,et al.  Detecting Non-Brownian Trait Evolution in Adaptive Radiations , 2006, PLoS biology.

[57]  J. Losos,et al.  Exceptional Convergence on the Macroevolutionary Landscape in Island Lizard Radiations , 2013, Science.

[58]  J. Felsenstein Phylogenies and quantitative characters , 1988 .

[59]  R. FitzJohn Diversitree: comparative phylogenetic analyses of diversification in R , 2012 .

[60]  R. Freckleton The seven deadly sins of comparative analysis , 2009, Journal of evolutionary biology.

[61]  S. Price,et al.  Tempo of trophic evolution and its impact on mammalian diversification , 2012, Proceedings of the National Academy of Sciences.

[62]  E. Martins The Comparative Method in Evolutionary Biology, Paul H. Harvey, Mark D. Pagel. Oxford University Press, Oxford (1991), vii, + 239 Price $24.95 paperback , 1992 .

[63]  William A. Walters,et al.  Evolutionary Inferences from Phylogenies: A Review of Methods , 2012 .

[64]  Ramón Díaz-Uriarte,et al.  TESTING HYPOTHESES OF CORRELATED EVOLUTION USING PHYLOGENETICALLY INDEPENDENT CONTRASTS: SENSITIVITY TO DEVIATIONS FROM BROWNIAN MOTION , 1996 .

[65]  R. Horres,et al.  Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. , 2014, Molecular phylogenetics and evolution.