Phylogenetic uncertainty revisited: Implications for ecological analyses

Ecologists and biogeographers usually rely on a single phylogenetic tree to study evolutionary processes that affect macroecological patterns. This approach ignores the fact that each phylogenetic tree is a hypothesis about the evolutionary history of a clade, and cannot be directly observed in nature. Also, trees often leave out many extant species, or include missing species as polytomies because of a lack of information on the relationship among taxa. Still, researchers usually do not quantify the effects of phylogenetic uncertainty in ecological analyses. We propose here a novel analytical strategy to maximize the use of incomplete phylogenetic information, while simultaneously accounting for several sources of phylogenetic uncertainty that may distort statistical inferences about evolutionary processes. We illustrate the approach using a clade‐wide analysis of the hummingbirds, evaluating how different sources of uncertainty affect several phylogenetic comparative analyses of trait evolution and biogeographic patterns. Although no statistical approximation can fully substitute for a complete and robust phylogeny, the method we describe and illustrate enables researchers to broaden the number of clades for which studies informed by evolutionary relationships are possible, while allowing the estimation and control of statistical error that arises from phylogenetic uncertainty. Software tools to carry out the necessary computations are offered.

[1]  Liang Liu,et al.  Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. , 2014, Systematic biology.

[2]  E. Cooper Overly simplistic substitution models obscure green plant phylogeny. , 2014, Trends in plant science.

[3]  R. Dudley,et al.  Molecular Phylogenetics and the Diversification of Hummingbirds , 2014, Current Biology.

[4]  S. Gouveia,et al.  Spatially explicit analyses highlight idiosyncrasies: species extinctions and the loss of evolutionary history , 2013 .

[5]  J. Diniz‐Filho,et al.  Darwinian shortfalls in biodiversity conservation. , 2013, Trends in ecology & evolution.

[6]  Thierson Couto,et al.  SUNPLIN: Simulation with Uncertainty for Phylogenetic Investigations , 2013, BMC Bioinformatics.

[7]  C. Ricotta,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN BIOLOGICAL TRAITS: THE UBIQUITY OF CROSS‐PRODUCT STATISTICS , 2013, Evolution; international journal of organic evolution.

[8]  W. Thuiller,et al.  Building megaphylogenies for macroecology: taking up the challenge. , 2013, Ecography.

[9]  W. Jetz,et al.  The global diversity of birds in space and time , 2012, Nature.

[10]  Nathan J B Kraft,et al.  Incompletely resolved phylogenetic trees inflate estimates of phylogenetic conservatism. , 2012, Ecology.

[11]  Tyler S. Kuhn,et al.  A simple polytomy resolver for dated phylogenies , 2011 .

[12]  Robert K. Colwell,et al.  A stochastic, evolutionary model for range shifts and richness on tropical elevational gradients under Quaternary glacial cycles , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  David Fernández-Baca,et al.  Robinson-Foulds Supertrees , 2010, Algorithms for Molecular Biology.

[14]  Richard G FitzJohn,et al.  Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. , 2009, Systematic biology.

[15]  J. L. Parra,et al.  Phylogenetic structure in tropical hummingbird communities , 2009, Proceedings of the National Academy of Sciences.

[16]  T. F. Hansen,et al.  A Comparative Method for Studying Adaptation to a Randomly Evolving Environment , 2008, Evolution; international journal of organic evolution.

[17]  L. Revell,et al.  Phylogenetic signal, evolutionary process, and rate. , 2008, Systematic biology.

[18]  J. Cotton,et al.  Tempo and Mode of Diversification of Lake Tanganyika Cichlid Fishes , 2008, PloS one.

[19]  Saltelli Andrea,et al.  Global Sensitivity Analysis: The Primer , 2008 .

[20]  J. Dunning,et al.  CRC Handbook of Avian Body Masses , 2007 .

[21]  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.

[22]  Sylvain Guillemot,et al.  PhySIC: a veto supertree method with desirable properties. , 2007, Systematic biology.

[23]  T. Garland,et al.  Within-species variation and measurement error in phylogenetic comparative methods. , 2007, Systematic biology.

[24]  N. Isaac,et al.  Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny , 2007, PloS one.

[25]  Matthew R. Helmus,et al.  Phylogenetic Measures of Biodiversity , 2007, The American Naturalist.

[26]  Luis A. Ortega,et al.  A NEW SPECIES OF ERIOCNEMIS (TROCHILIDAE) FROM SOUTHWEST COLOMBIA , 2007 .

[27]  Andy Purvis,et al.  A higher-level MRP supertree of placental mammals , 2006, BMC Evolutionary Biology.

[28]  D. Hillis,et al.  Analysis and visualization of tree space. , 2005, Systematic biology.

[29]  E. Vrba,et al.  A complete estimate of the phylogenetic relationships in Ruminantia: a dated species‐level supertree of the extant ruminants , 2005, Biological reviews of the Cambridge Philosophical Society.

[30]  K. Holsinger,et al.  Polytomies and Bayesian phylogenetic inference. , 2005, Systematic biology.

[31]  Campbell O. Webb,et al.  Phylomatic: tree assembly for applied phylogenetics , 2005 .

[32]  C. Simon,et al.  The Past and Future of Systematic Biology , 2005 .

[33]  Fredrik Ronquist,et al.  Bayesian Inference of Character Evolution , 2022 .

[34]  O. Bininda-Emonds,et al.  The evolution of supertrees. , 2004, Trends in ecology & evolution.

[35]  Pamela S Soltis,et al.  Darwin's abominable mystery: Insights from a supertree of the angiosperms , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  B. Rannala,et al.  DETECTING CORRELATION BETWEEN CHARACTERS IN A COMPARATIVE ANALYSIS WITH UNCERTAIN PHYLOGENY , 2003, Evolution; international journal of organic evolution.

[37]  M. Holder,et al.  Phylogeny estimation: traditional and Bayesian approaches , 2003, Nature Reviews Genetics.

[38]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[39]  E. Martins,et al.  Random sampling of constrained phylogenies: conducting phylogenetic analyses when the phylogeny is partially known. , 2001, Systematic biology.

[40]  J. Diniz‐Filho,et al.  PHYLOGENETIC AUTOCORRELATION UNDER DISTINCT EVOLUTIONARY PROCESSES , 2001, Evolution; international journal of organic evolution.

[41]  G. Graves,et al.  Multiscale assessment of patterns of avian species richness , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[43]  G. Graves,et al.  Detection of macro-ecological patterns in South American hummingbirds is affected by spatial scale , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  R. K. Colwell Rensch’s Rule Crosses the Line: Convergent Allometry of Sexual Size Dimorphism in Hummingbirds and Flower Mites , 2000, The American Naturalist.

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

[46]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[47]  J. L. Gittleman,et al.  Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia) , 1999, Biological reviews of the Cambridge Philosophical Society.

[48]  E. Abouheif RANDOM TREES AND THE COMPARATIVE METHOD: A CAUTIONARY TALE , 1998, Evolution; international journal of organic evolution.

[49]  David J. Pannell,et al.  Sensitivity Analysis of Normative Economic Models: Theoretical Framework and Practical Strategies , 1997 .

[50]  E. Martins CONDUCTING PHYLOGENETIC COMPARATIVE STUDIES WHEN THE PHYLOGENY IS NOT KNOWN , 1996, Evolution; international journal of organic evolution.

[51]  F. G. Stiles A New Species of Emerald Hummingbird (Trochilidae, Chlorostilbon) from the Sierra de Chiribiquete, Southeastern Colombia, with a Review of the C. mellisugus Complex , 1996 .

[52]  J. Losos An Approach to the Analysis of Comparative Data When a Phylogeny Is Unavailable or Incomplete , 1994 .

[53]  R. Tibshirani,et al.  An Introduction to the Bootstrap , 1995 .

[54]  M. Steel,et al.  Distributions of Tree Comparison Metrics—Some New Results , 1993 .

[55]  Robert Tibshirani,et al.  An Introduction to the Bootstrap CHAPMAN & HALL/CRC , 1993 .

[56]  D. Swofford When are phylogeny estimates from molecular and morphological data incongruent , 1991 .

[57]  Mark Kot,et al.  Adaptation: Statistics and a Null Model for Estimating Phylogenetic Effects , 1990 .

[58]  G. Graves Elevational correlates of speciation and intraspecific geographic variation in plumage in Andean forest birds , 1985 .

[59]  B. McNeil,et al.  Probabilistic Sensitivity Analysis Using Monte Carlo Simulation , 1985, Medical decision making : an international journal of the Society for Medical Decision Making.

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