Multivariate analyses of brain composition in mammals, amphibians and fish have revealed the evolution of ‘cerebrotypes’ that reflect specific niches and/or clades. Here, we present the first demonstration of similar cerebrotypes in birds. Using principal component analysis and hierarchical clustering methods to analyze a data set of 67 species, we demonstrate that five main cerebrotypes can be recognized. One type is dominated by galliforms and pigeons, among other species, that all share relatively large brainstems, but can be further differentiated by the proportional size of the cerebellum and telencephalic regions. The second cerebrotype contains a range of species that all share relatively large cerebellar and small nidopallial volumes. A third type is composed of two species, the tawny frogmouth (Podargus strigoides) and an owl, both of which share extremely large Wulst volumes. Parrots and passerines, the principal members of the fourth group, possess much larger nidopallial, mesopallial and striatopallidal proportions than the other groups. The fifth cerebrotype contains species such as raptors and waterfowl that are not found at the extremes for any of the brain regions and could therefore be classified as ‘generalist’ brains. Overall, the clustering of species does not directly reflect the phylogenetic relationships among species, but there is a tendency for species within an order to clump together. There may also be a weak relationship between cerebrotype and developmental differences, but two of the main clusters contained species with both altricial and precocial developmental patterns. As a whole, the groupings do agree with behavioral and ecological similarities among species. Most notably, species that share similarities in locomotor behavior, mode of prey capture or cognitive ability are clustered together. The relationship between cerebrotype and behavior/ecology in birds suggests that future comparative studies of brain-behavior relationships will benefit from adopting a multivariate approach.

Keywords:
Birds, Wulst, Nidopallium, Brainstem, Cerebellum, Evolution, Prey capture, Cognition
1.
Aldenderfer MS, Blashfield RK (1984) Cluster Analysis. Beverly Hills: Sage Publications.
2.
Ball GF, Balthazar J (2001) Ethological concepts revisited: immediate early gene induction in response to sexual stimuli in birds. Brain Behav Evol 57:252–270.
3.
Barber TA, Howorth PD, Klunk AM, Cho CC (1999) Lesions of the intermediate medial hyperstriatum ventrale impair sickness-conditioned learning in day-old chicks. Neurobiol Learn Mem 72:128–141.
4.
Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058.
5.
Barton RA, Aggleton JP, Grenyer R (2003) Evolutionary coherence of the mammalian amygdala. Proc R Soc Lond B 270:539–543.
6.
Bennett PM, Harvey PH (1985) Brain size, development and metabolism in birds and mammals. J Zool Lond 207:491–509.
7.
Bennett PM, Owens IPF (2002) Evolutionary Ecology of Birds: Life Histories, Mating Systems and Evolution. Oxford: Oxford University Press.
8.
Boire D (1989) Comparaison quantitative de l’éncephale de ses grades subdivisions et de relais visuals, trijumaux et acoustiques chez 28 especes. PhD Thesis, Université de Montreal, Montreal.
9.
Boire D, Baron G (1994) Allometric comparison of brain and main brain subdivisions in birds. J Brain Res 35:49–66.
10.
Bonke BA, Bonke D, Scheich H (1979) Connectivity of the auditory forebrain nuclei in the guinea fowl (Numida meleagris). Cell Tissue Res 200:101–121.
11.
Braun K, Bock J, Metzger M, Jiang S, Schnabel R (1999) The dorsocaudal neostriatum of the domestic chick: a structure serving higher associative functions. Behav Brain Res 98:211–218.
12.
Burish MJ, Kueh HY, Wang SS-H (2004) Brain architecture and social complexity in modern and ancient birds. Brain Behav Evol 63:107–124.
13.
Carezzano FJ, Bee de Speroni N (1995) Composicion volumetrica encefalica e indices cerebrales en tres aves de ambiente acuatico (Ardeidae, Podicipedidae, Rallidae). Facena 11:75–83.
14.
Christidis L, Schodde R, Shaw DD, Maynes SF (1991) Relationships among the Australo-Papuan parrots, lorikeets, and cockatoos (Aves: Psittaciformes): protein evidence. Condor 93:302–317.
15.
Clark DA, Mitra PP, Wang SS-H (2001) Scalable architecture in mammalian brains. Nature 411:189–193.
16.
Cleere N (1998) Nightjars: A Guide to the Nightjars, Nighthawks, and Their Relatives. New Haven, CT: Yale University Press.
17.
Csillag A (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav Brain Res 98:227–236.
18.
de Winter W, Oxnard CE (2001) Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409:710–714.
19.
Dimcheff DE, Drovetski SV, Mindell DP (2002) Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol Phylogenet Evol 24:203–215.
20.
Doré J-C, Ojasoo T, Thireau M (2002) Using the volumetric indices of telencephalic structures to distinguish Salamandridae and Plethodontidae: comparison of three statistical methods. J Theor Biol 214:427–439.
21.
Ebinger P (1995) Domestication and plasticity of brain organization in mallards (Anas platyrhynchos). Brain Behav Evol 45:286–300.
22.
Ebinger P, Löhmer R (1984) Comparative quantitative investigations on brains of rock doves, domestic and urban pigeons (Columba l. livia). Z Zool Syst Evolut-forsch 22:136–145.
23.
Ebinger P, Löhmer R (1987) A volumetric comparison of brains between greylag geese (Anser anser L.) and domestic geese. J Hirnforsch 3:291–299.
24.
Ebinger P, Röhrs M (1995) Volumetric analysis of brain structures, especially of the visual system in wild and domestic turkeys (Meleagris gallopavo). J Brain Res 36:219–228.
25.
Emery NJ, Clayton NS (2004) Comparing the complex cognition of birds and primates. In: Comparative Vertebrate Cognition (Rogers LJ, Kaplan G, eds), pp 3–55. New York: Kluwer Academic/Plenum Publishers.
26.
Feduccia A (1999) The Origin and Evolution of Birds. 2nd edition. New Haven, CT: Yale University Press.
27.
Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584.
28.
Finlay BL, Darlington RB, Nicastro N (2001) Developmental structure in brain evolution. Behav Brain Sci 24:263–308.
29.
Fry CH, Fry K (1992) Kingfishers, Bee-eaters and Rollers. Princeton, NJ: Princeton University Press.
30.
Gentner TQ, Hulse SH, Bentley GE, Ball GF (2000) Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J Neurobiol 42:117–133.
31.
Güntürkün O, Durstewitz D (2000) Multimodal areas of the avian forebrain – blueprints for cognition? In: Brain Evolution and Cognition (Roth G, Wullimann MF, eds), pp 431–450. New York: John Wiley and Sons.
32.
Horn G (1998) Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci 21:300–305.
33.
Huber R, van Staaden MJ, Kaufman LS, Liem KF (1997) Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167–182.
34.
Husband S, Shimizu T (2001) Evolution of the avian visual system. In: Avian Visual Cognition. (Cook RG, ed). Medford, MA: Tufts University. E-book available from http://www.pigeon.psy.tufts.edu/avc/husband/
35.
Ihaka R, Gentleman R (1996) R: A language for data analysis and graphics. J Comp Graph Stats 5:299–314.
36.
Iwaniuk AN (2003) The evolution of brain size and structure in birds. Unpublished PhD thesis, Monash University, Clayton, Australia.
37.
Iwaniuk AN, Arnold KE (2004) Is cooperative breeding associated with bigger brains? A comparative test in the Corvida (Passeriformes). Ethology 110:203–220.
38.
Iwaniuk AN, Nelson JE (2002) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928.
39.
Iwaniuk AN, Dean KM, Nelson JE (2005) Allometry of the brain and brain regions in parrots (Psittaciformes): comparisons with other birds and primates. Brain Behav Evol 65:40–59.
40.
Iwaniuk AN, Dean KM, Nelson JE (2004) A mosaic pattern characterizes the evolution of the avian brain. Proc R Soc Lond B 271:S148–S151.
41.
Kimball RT, Braun EL, Zwartjes PW, Crowe TM, Ligon JD (1999) A molecular phylogeny of the pheasants and partridges suggests that these lineages are not monophyletic. Mol Phylogenet Evol 11:38–54.
42.
Kroner S, Güntürkün O (1999) Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): a retro- and anterograde pathway tracing study. J Comp Neurol 407:228–260.
43.
Kubke MF, Massoglia DP, Carr CE (2004) Bigger brains or bigger nuclei? Regulating the size of auditory structures in birds. Brain Behav Evol 63:169–180.
44.
Lapointe F-J, Baron G, Legendre P (1999) Encephalization, adaptation and evolution of Chiroptera: A statistical analysis with further evidence for bat monophyly. Brain Behav Evol 54:1191–1226.
45.
Lefebvre L, Gaxiola A, Dawson S, Timmermans S, Rosza L, Kabai P (1998) Feeding innovations and forebrain size in Australasian birds. Behaviour 135:1077–1097.
46.
Lefebvre L, Nicolakakis N, Boire, D (2002) Tools and brains in birds. Behaviour 139:939–973.
47.
Lefebvre L, Whittle PW, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:549–560.
48.
Legendre P, Lapointe F-J, Casgrain P (1994) Modeling brain evolution from behavior: a permutational regression approach. Evolution 48:1487–1499.
49.
Marler PM (1996) Social cognition: Are primates smarter than birds? Curr Ornithol 13:1–32.
50.
Mayr G (2002) Osteological evidence for paraphyly of the avian order Caprimulgiformes (nightjars and allies). J Ornithol 143:82–97.
51.
Monroe BL, Jr, Sibley CG (1997) A World Checklist of Birds. New Haven, CT: Yale University Press.
52.
Moroney MK, Pettigrew JD (1987) Some observations on the visual optics of kingfishers (Aves, Coraciformes, Alcedinidae). J Comp Physiol A 160:137–149.
53.
Murtagh F (1985) Multidimensional Clustering Algorithms. Heidelberg and Vienna: Physica-Verlag.
54.
Nealen PM, Ricklefs RE (2001) Early diversification of the avian brain:body relationship. J Zool Lond 253:391–404.
55.
Nguyen AP, Spetch ML, Crowder NA, Winship IR, Hurd PL, Wylie DRW (2004) A dissociation of motion and spatial-pattern vision in the avian telencephalon: implications for the evolution of ‘visual streams’. J Neurosci 24:4962–4970.
56.
Pettigrew JD (1986) Evolution of binocular vision. In: Visual Neuroscience (Sanderson KJ, Levick WR, eds.), pp 208–222. Cambridge, UK: Cambridge University Press.
57.
Plummer TK, Striedter GF (2002) Brain lesions that impair vocal imitation in adult budgerigars. J Neurobiol 53:413–428.
58.
Price EO (1984) Behavioral aspects of animal domestication. Q Rev Biol 59:1–32.
59.
Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271.
60.
Rehkämper G, Frahm HD, Zilles K (1991) Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (insectivores and primates). Brain Behav Evol 37:125–143.
61.
Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Güntürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414.
62.
Ribeiro S, Cecchi GA, Magnasco MO, Mello CV (1998) Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 21:359–371.
63.
Ridet J-M, Bauchot R (1991) Analyse quantitative de l’encéphale des téléostéens: caractères évolutifs et adaptifs de l’encéphalisation. III. Analyse multivariée des indices encéphaliques. J Hirnforsch 32:439–449.
64.
Rohlf FJ (1970) Adaptive hierarchical clustering schemes. Syst Zool 19:58–82.
65.
Scharff C, Nottebohm (1991) A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J Neurosci 11:2896–2913.
66.
Shapiro B, Sibthorpe D, Rambaut A, Austin J, Wragg GM, Bininda-Emonds OR, Lee PL, Cooper A (2002) Flight of the dodo. Science 295:1683.
67.
Sibley CG, Ahlquist JE (1990) Phylogeny and Classification of Birds. New Haven, CT: Yale University Press.
68.
Sossinska R (1982) Domestication in birds. In: Avian Biology, Volume VI, (Farner DS, King JR, Parkes, KC, eds.), pp 373–403. New York: Academic Press.
69.
Sultan F (2002) Analysis of mammalian brain architecture. Nature 415:133–134.
70.
Timmermans S, Lefebvre L, Boire D, Basu P (2000) Relative size of the hyperstriatum ventrale is the the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203.
71.
Venables WN, Ripley BD (1999) Modern Applied Statistics With S-Plus. New York: Springer-Verlag.
72.
Wagner H-J (2001a) Sensory brain areas in mesopelagic fishes. Brain Behav Evol 57:117–133.
73.
Wagner H-J (2001b) Brain areas in abyssal demersal fishes. Brain Behav Evol 57:301–316.
74.
Wallman J, Pettigrew JD (1985) Conjugate and disjunctive saccades in two avian species with contrasting oculomotor strategies. J Neurosci 5:1418–1428.
75.
Watanabe S (2001) Effects of lobus paraolfactorius lesions on repeated acquisition of spatial discrimination in pigeons. Brain Behav Evol 58:333–342.
76.
Whiting BA, Barton RA (2003) The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J Hum Evol 44:3–10.
77.
Wild JM, Reinke H, Farabaugh SM (1997) A non-thalamic pathway contributes to a whole body map in the brain of the budgerigar. Brain Res 755:137–141.
© 2005 S. Karger AG, Basel
2005
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.