Brains, tools, innovation and biogeography in crows and ravens

BackgroundCrows and ravens (Passeriformes: Corvus) are large-brained birds with enhanced cognitive abilities relative to other birds. They are among the few non-hominid organisms on Earth to be considered intelligent and well-known examples exist of several crow species having evolved innovative strategies and even use of tools in their search for food. The 40 Corvus species have also been successful dispersers and are distributed on most continents and in remote archipelagos.ResultsThis study presents the first molecular phylogeny including all species and a number of subspecies within the genus Corvus. We date the phylogeny and determine ancestral areas to investigate historical biogeographical patterns of the crows. Additionally, we use data on brain size and a large database on innovative behaviour and tool use to test whether brain size (i) explains innovative behaviour and success in applying tools when foraging and (ii) has some correlative role in the success of colonization of islands. Our results demonstrate that crows originated in the Palaearctic in the Miocene from where they dispersed to North America and the Caribbean, Africa and Australasia. We find that relative brain size alone does not explain tool use, innovative feeding strategies and dispersal success within crows.ConclusionsOur study supports monophyly of the genus Corvus and further demonstrates the direction and timing of colonization from the area of origin in the Palaearctic to other continents and archipelagos. The Caribbean was probably colonized from North America, although some North American ancestor may have gone extinct, and the Pacific was colonized multiple times from Asia and Australia. We did not find a correlation between relative brain size, tool use, innovative feeding strategies and dispersal success. Hence, we propose that all crows and ravens have relatively large brains compared to other birds and thus the potential to be innovative if conditions and circumstances are right.

[1]  Harry F. Recher,et al.  On the Relation between Habitat Selection and Species Diversity , 1966, The American Naturalist.

[2]  Campbell O. Webb,et al.  A LIKELIHOOD FRAMEWORK FOR INFERRING THE EVOLUTION OF GEOGRAPHIC RANGE ON PHYLOGENETIC TREES , 2005, Evolution; international journal of organic evolution.

[3]  R. Ricklefs,et al.  Major global radiation of corvoid birds originated in the proto-Papuan archipelago , 2011, Proceedings of the National Academy of Sciences.

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

[5]  Nicola S. Clayton,et al.  The Mentality of Crows: Convergent Evolution of Intelligence in Corvids and Apes , 2004, Science.

[6]  A. Gamauf,et al.  Phylogeographic patterns in widespread corvid birds. , 2007, Molecular phylogenetics and evolution.

[7]  Louis Lefebvre,et al.  Technical innovations drive the relationship between innovativeness and residual brain size in birds , 2009, Animal Behaviour.

[8]  S. Hackett Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). , 1996, Molecular phylogenetics and evolution.

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

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

[11]  Artin,et al.  Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World suboscines ( Aves , Passeriformes ) , 2006 .

[12]  D. Goodwin,et al.  Crows of the world , 1976 .

[13]  K. E. Omland,et al.  NOVEL INTRON PHYLOGENY SUPPORTS PLUMAGE CONVERGENCE IN ORIOLES (ICTERUS) , 2003 .

[14]  Derrick J. Zwickl Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion , 2006 .

[15]  J. Nelson,et al.  Developmental differences are correlated with relative brain size in birds: a comparative analysis , 2003 .

[16]  A. Kacelnik,et al.  Behavioural ecology: Tool manufacture by naive juvenile crows , 2005, Nature.

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

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

[19]  J. Losos,et al.  EVOLUTIONARY CONSEQUENCES OF ECOLOGICAL RELEASE IN CARIBBEAN ANOLIS LIZARDS , 1997 .

[20]  Alexei J Drummond,et al.  Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. , 2002, Genetics.

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

[22]  K. Hammerschmidt,et al.  Calls of the Jungle Crow (Corvus macrorhynchos s.l.) as a taxonomic character , 2000, Journal für Ornithologie.

[23]  R. Bowie,et al.  Repeated trans‐Atlantic dispersal catalysed a global songbird radiation , 2009 .

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

[25]  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.

[26]  J. Marzluff,et al.  Cryptic genetic variation and paraphyly in ravens , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  L. Lefebvre Taxonomic counts of cognition in the wild , 2011, Biology Letters.

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

[29]  Joel Cracraft,et al.  Phylogeny and diversification of the largest avian radiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[31]  J. Ekman,et al.  Inter-generic relationships of the crows, jays, magpies and allied groups (Aves: Corvidae) based on nucleotide sequence data , 2005 .

[32]  M. Audley-Charles,et al.  Tectonics of the New Guinea Area , 1991 .

[33]  D. Schluter,et al.  Calibrating the avian molecular clock , 2008, Molecular ecology.

[34]  C. Cicero,et al.  Higher-level phylogeny of new world vireos (aves: vireonidae) based on sequences of multiple mitochondrial DNA genes. , 2001, Molecular phylogenetics and evolution.

[35]  M. Donoghue,et al.  Combining historical biogeography with niche modeling in the Caprifolium clade of Lonicera (Caprifoliaceae, Dipsacales). , 2010, Systematic biology.

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

[37]  L. Lefebvre,et al.  Feeding innovations and forebrain size in birds , 1997, Animal Behaviour.

[38]  S. Ho Calibrating molecular estimates of substitution rates and divergence times in birds , 2007 .

[39]  S. Goodacre,et al.  Biogeography of the fauna of French Polynesia: diversification within and between a series of hot spot archipelagos , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[41]  K. Bickart The birds of the late Miocene-early Pliocene Big Sandy Formation, Mohave County, Arizona , 1990 .

[42]  M. Källersjö,et al.  Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World suboscines (Aves, Passeriformes) , 2006 .

[43]  J. Fjeldså,et al.  Sapayoa aenigma: a New World representative of 'Old World suboscines' , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  R. Chesser Molecular Systematics of the Rhinocryptid Genus Pteroptochos , 1999 .

[45]  I. Rowley A Fourth Species of Australian Corvid , 1967 .

[46]  G. Hunt Manufacture and use of hook-tools by New Caledonian crows , 1996, Nature.

[47]  L. Marino Convergence of Complex Cognitive Abilities in Cetaceans and Primates , 2002, Brain, Behavior and Evolution.

[48]  Daniel Sol,et al.  Behavioural flexibility and invasion success in birds , 2002, Animal Behaviour.

[49]  Candy Rowe,et al.  A critique of comparative studies of brain size , 2007, Proceedings of the Royal Society B: Biological Sciences.

[50]  Christian Rutz,et al.  The Ecological Significance of Tool Use in New Caledonian Crows , 2010, Science.

[51]  Russell D. Gray,et al.  Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides) , 2008, Neuroscience Letters.

[52]  J. Holloway,et al.  Biogeography and geological evolution of se Asia , 1998 .

[53]  S. Hackett Molecular Phylogenetics and Biogeography of Tanagers in the GenusRamphocelus(Aves) , 1996 .

[54]  P H Harvey,et al.  Comparing brains. , 1990, Science.

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

[56]  Louis Lefebvre,et al.  Tools and brains in birds , 2002 .

[57]  L. Lefebvre,et al.  Big brains, enhanced cognition, and response of birds to novel environments. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Michael Tomasello,et al.  Primate Cognition , 2010, Top. Cogn. Sci..

[59]  V. Bentley-Condit,et al.  Animal tool use: current definitions and an updated comprehensive catalog , 2010 .

[60]  M. Pagel,et al.  Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence , 2002, The American Naturalist.

[61]  J. Marzluff,et al.  Social learning spreads knowledge about dangerous humans among American crows , 2012, Proceedings of the Royal Society B: Biological Sciences.

[62]  L. Lefebvre,et al.  Brains, Lifestyles and Cognition: Are There General Trends? , 2008, Brain, Behavior and Evolution.

[63]  John Wakeley,et al.  Estimating Divergence Times from Molecular Data on Phylogenetic and Population Genetic Timescales , 2002 .

[64]  S. Tebbich,et al.  Do woodpecker finches acquire tool-use by social learning? , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[65]  R. Macarthur,et al.  On Optimal Use of a Patchy Environment , 1966, The American Naturalist.