Bigger is not always better: when brains get smaller
Abstract
Many studies assume that an increase in brain size is beneficial. However, the costs of producing and maintaining a brain are high, and we argue that brain size should be secondarily reduced by natural selection whenever the costs outweigh the benefits. Our results confirm this by showing that brain size is subject to bidirectional selection. Relative to the ancestral state, brain size in bats has been reduced in fast flyers, while it has increased in manoeuvrable flyers adapted to flight in complex habitats. This study emphasizes that brain reduction and enlargement are equally important, and they should both be considered when investigating brain size evolution.
References
Aiello L.C& Wheeler P . 1995The expensive-tissue hypothesis—the brain and the digestive-system in human and primate evolution. Curr. Anthropol 36, 199–221.doi:10.1086/204350. Crossref, ISI, Google ScholarAltshuler D.L& Dudley R . 2002The ecological and evolutionary interface of hummingbird flight physiology. J. Exp. Biol 205, 2325–2336. Crossref, PubMed, ISI, Google ScholarAschoff J, Günther B& Kramer K . 1971Energiehaushalt und Temperaturregulation. München:Urban and Schwarzenberg. Google ScholarBaron G, Stephan H& Frahm H.D . 1996Comparative neurobiology in Chiroptera. Basel:Birkhäuser. Google ScholarBarton R.A& Harvey P.H . 2000Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058.doi:10.1038/35016580. Crossref, PubMed, ISI, Google ScholarBerger M& Hart J.S . 1974Physiology and energetics of flight., Farner D.S& King J.R In Avian biology vol. IVNew York:Academic Press260–415. Google ScholarBrenowitz E.A . 2004Plasticity of the adult avian song control system. Ann. NY Acad. Sci 1016, 560–585.doi:10.1196/annals.1298.006. Crossref, PubMed, ISI, Google ScholarDiaz-Uriarte R& Garland T . 1998Effects of branch length errors on the performance of phylogenetically independent contrasts. Syst. Biol 47, 654–672.doi:10.1080/106351598260653. Crossref, PubMed, ISI, Google ScholarEisenberg J.F& Wilson D.E . 1978Relative brain size and feeding strategies in the Chiroptera. Evolution 32, 740–751. Crossref, PubMed, ISI, Google ScholarFelsenstein J . 1985Phylogenies and the comparative method. Am. Nat 125, 1–15.doi:10.1086/284325. Crossref, ISI, Google ScholarFinlay B.L& Darlington R.B . 1995Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584. Crossref, PubMed, ISI, Google ScholarGarland T, Harvey P.H& Ives A.R . 1992Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol 41, 18–32. Crossref, ISI, Google ScholarHarvey P.H& Krebs J.R . 1990Comparing brains. Science 249, 140–146. Crossref, PubMed, ISI, Google ScholarHutcheon J.M, Kirsch J.W& Garland T . 2002A comparative analysis of brain size in relation to foraging ecology and phylogeny in the Chiroptera. Brain Behav. Evol 60, 165–180.doi:10.1159/000065938. Crossref, PubMed, ISI, Google ScholarJones K.E& MacLarnon A.M . 2004Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat 164, E20–E31.doi:10.1086/421334. Crossref, PubMed, ISI, Google ScholarMartin R.D . 1981Relative brain size and basal metabolic-rate in terrestrial vertebrates. Nature 293, 57–60.doi:10.1038/293057a0. Crossref, PubMed, ISI, Google ScholarNorberg U.M . 1989Ecological determinants of bat wing shape and echolocation call structure with implications for some fossil bats., Hanàk V, Horàcek T& Gaisler J In European bat research 1987Prague:Charles University Press197–211. Google ScholarNorberg U.M& Rayner J.M.V . 1987Ecological morphology and flight in bats (Mammalia, Chiroptera)—wing adaptations, flight performance, foraging strategy and echolocation. Phil. Trans. R. Soc. B 316, 337–419. Link, ISI, Google ScholarPagel M . 1994Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. B 255, 37–45. Link, ISI, Google ScholarPagel M . 1997Inferring evolutionary processes from phylogenies. Zool. Scr 26, 331–348.doi:10.1111/j.1463-6409.1997.tb00423.x. Crossref, ISI, Google ScholarPagel M Inferring the historical patterns of biological evolution. Nature 4011999a877–884.doi:10.1038/44766. Crossref, PubMed, ISI, Google ScholarPagel M The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol 481999b612–622.doi:10.1080/106351599260184. Crossref, ISI, Google ScholarPurvis A& Rambaut A . 1995Comparative-analysis by independent contrasts (CAIC)—an Apple-Macintosh application for analyzing comparative data. Comput. Appl. Biosci 11, 247–251. PubMed, Google ScholarSafi K& Dechmann D.K.N . 2005Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proc. R. Soc. B 272, 179–186.doi:10.1098/rspb.2004.2924doi:10.1098/rspb.2004.2924. Link, ISI, Google ScholarSimmons N.B& Geisler J.H . 1998Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist4–182. ISI, Google ScholarTobalske B.W, Hedrick T.L, Dial K.P& Biewener A.A . 2003Comparative power curves in bird flight. Nature 421, 363–366.doi:10.1038/nature01284. Crossref, PubMed, ISI, Google Scholar



