Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy.

Hummingbirds are an important model system in avian biology, but to date the group has been the subject of remarkably few phylogenetic investigations. Here we present partitioned Bayesian and maximum likelihood phylogenetic analyses for 151 of approximately 330 species of hummingbirds and 12 outgroup taxa based on two protein-coding mitochondrial genes (ND2 and ND4), flanking tRNAs, and two nuclear introns (AK1 and BFib). We analyzed these data under several partitioning strategies ranging between unpartitioned and a maximum of nine partitions. In order to select a statistically justified partitioning strategy following partitioned Bayesian analysis, we considered four alternative criteria including Bayes factors, modified versions of the Akaike information criterion for small sample sizes (AIC(c)), Bayesian information criterion (BIC), and a decision-theoretic methodology (DT). Following partitioned maximum likelihood analyses, we selected a best-fitting strategy using hierarchical likelihood ratio tests (hLRTS), the conventional AICc, BIC, and DT, concluding that the most stringent criterion, the performance-based DT, was the most appropriate methodology for selecting amongst partitioning strategies. In the context of our well-resolved and well-supported phylogenetic estimate, we consider the historical biogeography of hummingbirds using ancestral state reconstructions of (1) primary geographic region of occurrence (i.e., South America, Central America, North America, Greater Antilles, Lesser Antilles), (2) Andean or non-Andean geographic distribution, and (3) minimum elevational occurrence. These analyses indicate that the basal hummingbird assemblages originated in the lowlands of South America, that most of the principle clades of hummingbirds (all but Mountain Gems and possibly Bees) originated on this continent, and that there have been many (at least 30) independent invasions of other primary landmasses, especially Central America.

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

[2]  T. Castoe,et al.  Modeling nucleotide evolution at the mesoscale: the phylogeny of the neotropical pitvipers of the Porthidium group (viperidae: crotalinae). , 2005, Molecular phylogenetics and evolution.

[3]  W. Maddison.  Squared-Change Parsimony Reconstructions of Ancestral States for Continuous-Valued Characters on a Phylogenetic Tree , 1991 .

[4]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[5]  J. Lighton,et al.  Oxygen consumption during hover-feeding in free-ranging Anna hummingbirds. , 1986, The Journal of experimental biology.

[6]  J. Macey,et al.  Re: Homology in phylogenetic analysis: alignment of transfer RNA genes and the phylogenetic position of snakes. , 1997, Molecular phylogenetics and evolution.

[7]  W. Moore,et al.  The utility of DNA sequences of an intron from the beta-fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae). , 1997, Molecular phylogenetics and evolution.

[8]  M. Nishida,et al.  Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics , 1993, Journal of Molecular Evolution.

[9]  G. Lowery.  The Species of Birds of South America and Their Distribution Rodolphe Meyer de Schauensee , 1969 .

[10]  James E. Byers,et al.  MODEL SELECTION IN PHYLOGENETICS , 2005 .

[11]  J. Lighton,et al.  Mitochondrial respiration in hummingbird flight muscles. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[13]  R. Dudley,et al.  Limits to flight energetics of hummingbirds hovering in hypodense and hypoxic gas mixtures. , 1996, The Journal of experimental biology.

[14]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[15]  Joseph T. Chang,et al.  Full reconstruction of Markov models on evolutionary trees: identifiability and consistency. , 1996, Mathematical biosciences.

[16]  D. Mindell,et al.  Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. , 1999, Molecular phylogenetics and evolution.

[17]  D. Swofford,et al.  Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNA. , 2004, Molecular phylogenetics and evolution.

[18]  F. Chapman.  The distribution of bird-life in Ecuador ; a contribution to a study of the origin of Andean bird-life , 1927 .

[19]  R. Dudley,et al.  Resolution of a paradox: hummingbird flight at high elevation does not come without a cost. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

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

[22]  D. Schluter,et al.  LIKELIHOOD OF ANCESTOR STATES IN ADAPTIVE RADIATION , 1997, Evolution; international journal of organic evolution.

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

[24]  P. Stephens,et al.  REPLICATE PATTERNS OF SPECIES RICHNESS, HISTORICAL BIOGEOGRAPHY, AND PHYLOGENY IN HOLARCTIC TREEFROGS , 2005, Evolution; international journal of organic evolution.

[25]  Zaid Abdo,et al.  Performance-based selection of likelihood models for phylogeny estimation. , 2003, Systematic biology.

[26]  T. Castoe,et al.  Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). , 2006, Molecular phylogenetics and evolution.

[27]  J. Huelsenbeck,et al.  Bayesian phylogenetic analysis of combined data. , 2004, Systematic biology.

[28]  Sandhya Dwarkadas,et al.  Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference , 2002, Bioinform..

[29]  Hummingbirds and Their Flowers. , 1969 .

[30]  R. Bleiweiss.  Origin of hummingbird faunas , 1998 .

[31]  G. Mayr.  New specimens of the early Oligocene Old World hummingbird Eurotrochilus inexpectatus , 2007, Journal of Ornithology.

[32]  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.

[33]  J. Cracraft,et al.  Phylogenetic relationships among modern birds (Neornithes): towards an avian tree of life , 2004 .

[34]  D. Lack.  Island biology: Illustrated by the land birds of Jamaica , 1976 .

[35]  Mike Steel,et al.  Should phylogenetic models be trying to "fit an elephant"? , 2005, Trends in genetics : TIG.

[36]  J. Dumbacher,et al.  Adenylate Kinase Intron 5: A New Nuclear Locus for Avian Systematics , 2001 .

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

[38]  F. Chapman.  Remarks on the life zones of northeastern Venezuela with descriptions of new species of birds. American Museum novitates ; no. 191 , 1925 .

[39]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[40]  G. Mayr,et al.  PHYLOGENY OF EARLY TERTIARY SWIFTS AND HUMMINGBIRDS (AVES: APODIFORMES) , 2003 .

[41]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[42]  J H Sage,et al.  AMERICAN ORNITHOLOGISTS' UNION. , 1895, Science.

[43]  Check-List of Birds of the World , 1931, Nature.

[44]  W. Kress,et al.  Adaptation in a Plant-Hummingbird Association , 2003, Science.

[45]  P. Lewis,et al.  Success of maximum likelihood phylogeny inference in the four-taxon case. , 1995, Molecular biology and evolution.

[46]  E. Coues.  A Check List of North American Birds , 2009 .

[47]  M. Braun,et al.  The Avifauna of the Huancabamba Region, Northern Peru , 1985 .

[48]  J. Fitzpatrick.  Check-List of North American Birds. Sixth edition , 1984 .

[49]  J. Dickinson,et al.  Check-List of North American Birds , 1958 .

[50]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .

[51]  R. Dudley,et al.  Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox , 1995, Nature.

[52]  D. Barker,et al.  Evolutionary history of vegetative reproduction in Porpidia s.L. (Lichen-forming ascomycota). , 2006, Systematic biology.

[53]  K. Able.  Handbook of the Birds of the World, Volume 5, Barn-owls to Hummingbirds , 2000 .

[54]  A. Kratter,et al.  The Howard and Moore Complete Checklist of the Birds of the World , 2005 .

[55]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[56]  D. Lack.  THE NUMBERS OF SPECIES OF HUMMINGBIRDS IN THE WEST INDIES , 1973, Evolution; international journal of organic evolution.

[57]  J. Cracraft.  Historical Biogeography and Patterns of Differentiation within the South American Avifauna: Areas of Endemism , 1985 .

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

[59]  Mark Pagel,et al.  Major fungal lineages are derived from lichen symbiotic ancestors , 2022 .

[60]  G. Mayr.  Old World Fossil Record of Modern-Type Hummingbirds , 2004, Science.

[61]  Emily C. Moriarty,et al.  The importance of proper model assumption in bayesian phylogenetics. , 2004, Systematic biology.

[62]  C. Simon,et al.  Accurate branch length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch length priors. , 2006, Systematic biology.

[63]  D. Posada,et al.  Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. , 2004, Systematic biology.

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

[65]  H. Philippe,et al.  Computing Bayes factors using thermodynamic integration. , 2006, Systematic biology.

[66]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[67]  D. Swofford,et al.  Should we use model-based methods for phylogenetic inference when we know that assumptions about among-site rate variation and nucleotide substitution pattern are violated? , 2001, Systematic biology.

[68]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[69]  G. Gottsberger,et al.  The Hummingbird Plant Community of a Tropical Montane Rain Forest in Southern Ecuador , 2003 .

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

[71]  Kamaljit S. Bawa,et al.  La Selva: ecology and natural history of a neotropical rain forest. , 1995 .

[72]  Robert Dudley,et al.  The ecological and evolutionary interface of hummingbird flight physiology. , 2002, The Journal of experimental biology.

[73]  Zaid Abdo,et al.  Accounting for uncertainty in the tree topology has little effect on the decision-theoretic approach to model selection in phylogeny estimation. , 2005, Molecular biology and evolution.

[74]  J. S. Rogers,et al.  Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. , 2001, Systematic biology.

[75]  Joel Cracraft,et al.  Assembling the tree of life , 2004 .

[76]  R. Bleiweiss,et al.  DNA hybridization evidence for the principal lineages of hummingbirds (Aves:Trochilidae). , 1997, Molecular biology and evolution.

[77]  E C Dickinson,et al.  THE HOWARD AND MOORE COMPLETE CHECKLIST OF THE BIRDS OF THE WORLD. 4 th EDITION VOLUME 2 (2014) , 2003 .

[78]  O. Madsen,et al.  Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. , 2005, Systematic biology.

[79]  J. Huelsenbeck.  Performance of Phylogenetic Methods in Simulation , 1995 .

[80]  Variation Of A Muscle In Hummingbirds And Swifts And Its Systematic Implications , 1982 .

[81]  J. Wiens,et al.  Hylid frog phylogeny and sampling strategies for speciose clades. , 2005, Systematic biology.

[82]  B. Young,et al.  Neotropical Birds: Ecology and Conservation , 1996 .

[83]  James L. Peters.  Check-List of the Birds of the World. Volume V , 1946 .

[84]  R. Suarez,et al.  Oxygen and the upper limits to animal design and performance. , 1998, The Journal of experimental biology.

[85]  M. Pagel,et al.  A phylogenetic mixture model for detecting pattern-heterogeneity in gene sequence or character-state data. , 2004, Systematic biology.

[86]  J. Cracraft,et al.  Reconsideration of the phylogenetic relationships of the enigmatic Bornean Bristlehead (Pityriasis gymnocephala). , 2006, Molecular phylogenetics and evolution.

[87]  S. Herzog,et al.  Distribution and Flowering Ecology of Bromeliads along Two Climatically Contrasting Elevational Transects in the Bolivian Andes 1 , 2006 .

[88]  J. Sites,et al.  Mitochondrial DNA Sequence Divergence and Phylogenetic Relationships among Eight Chromosome Races of the Sceloporus Grammicus Complex (Phrynosomatidae) in Central Mexico , 1994 .

[89]  F. G. Stiles,et al.  GEOGRAPHICAL ASPECTS OF BIRD-FLOWER COEVOLUTION, WITH PARTICULAR REFERENCE TO CENTRAL AMERICA' , 1981 .

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

[91]  Museum Novitates.  REMARKS ON THE LIFE ZONES OF NORTHESASTERN VENEZUELA WITH DESCRIPTIONS OF NEW SPECIES OF BIRDS , 2004 .

[92]  David L. Swofford,et al.  Are Guinea Pigs Rodents? The Importance of Adequate Models in Molecular Phylogenetics , 1997, Journal of Mammalian Evolution.

[93]  Hummingbirds and their flowers , 1970 .

[94]  B. Rannala.  Identi(cid:142)ability of Parameters in MCMC Bayesian Inference of Phylogeny , 2002 .