The current paper details our developing understanding of the evolution of large brains in mammals. In order to do this, we first define brains that we consider to be large - those that have passed the apparent 700-gram ceiling on brain mass evolution in the class Mammalia. The over-700-gram club includes certain species within the genus Homo, order Cetacea, order Proboscidea, and suborder Pinnipedia. Our analysis suggests that selection for body size appears to be the most important factor in the evolution of large brain size, but there also appear to be internal morphophysiological constraints on large brain size evolution that need to be overcome in order for brains to break the 700-gram barrier. These two aspects appear to be common themes in the evolution of large brains. This significantly diminishes the explanatory value of selection for greater cognitive capacities as a principal factor in the evolution of enlarged brain sizes above the 700-gram threshold.

Keywords:
Human, Elephant, Cetacean, Pinniped, Brain evolution, Mammal
1.
Amatrudo JM, Weaver CM, Crimins JL, Hof PR, Rosene DL, Luebke JI (2012): Influence of highly distinctive structural properties on the excitability of pyramidal neurons in monkey visual and prefrontal cortices. J Neurosci 32:13644-13660.
2.
Bianchi S, Bauernfeind A, Stimpson C, Bonar C, Manger PR, Hof PR, Jacobs B, Sherwood CC (2011): Neuronal diversity in Afrotheria: a Golgi study of the rock hyrax (Procavia capensis) neocortex and comparison with the African elephant (Loxodonta africana). Ann NY Acad Sci 1225:37-46.
3.
Bininda-Emonds OR, Gittleman JL, Kelly CK (2001): Flippers versus feet: comparative trends in aquatic and non-aquatic carnivores. J Anim Ecol 70:386-400.
4.
Bininda-Emonds OR, Gittleman JL, Purvis A (1999): Building large trees by combining phylogenetic information: a complex phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143-175.
5.
Conroy GC, Smith RL (2007): The size of scalable brain components in the human evolutionary lineage: with a comment on the paradox of Homo floresiensis. Homo 58:1-12.
6.
Cozzi B, Spagnoli S, Bruno L (2001): An overview of the central nervous system of the elephant through a critical appraisal of the literature published in the XIX and XX centuries. Brain Res Bull 54:219-227.
7.
Crile G, Quiring DP (1940): A record of body weight and certain organ and gland weights of 3,690 animals. Ohio J Sci 40:219-259.
8.
Dart RE (1923): The brain of the Zeuglodontidae (Cetacea). Proc Zool Soc Lond 1923:615-654.
9.
Dell LA, Patzke N, Bhagwandin A, Bux F, Fuxe K, Barber G, Siegel JM, Manger PR (2012): Organization and number of orexinergic neurons in the hypothalamus of two species of Cetartiodactyla: a comparison of giraffe (Giraffe camelopardalis) and harbour porpoise (Phocoena phocoena). J Chem Neuroanat 44:98-109.
10.
Donhoffer SZ (1980): Homeothermia of the Brain. Budapest, Akadémiai Kiadó.
11.
Edinger T (1975): Paleoneurology 1804-1966: an annotated bibliography. Adv Anat Embryol Cell Biol 49:1-258.
12.
Elston GN (2000): Pyramidal cells of the frontal lobe: all the more spinous to think with. J Neurosci 20:91-94.
13.
Elston GN (2003a): Pyramidal cell heterogeneity in the visual cortex of the nocturnal new world owl monkey (Aotus trivirgatus). Neuroscience 117:213-219.
14.
Elston GN (2003b): The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): regional specialization in cell structure. Eur J Neurosci 17:1313-1318.
15.
Elston GN (2007): Specializations in pyramidal cell structure during primate evolution; in Kaas JH, Preuss TM (eds): Evolution of Nervous Systems. Oxford, Academic Press, pp 191-242.
16.
Elston GN, Benavides-Piccione R, DeFelipe J (2001): The pyramidal cell in cognition: a comparative study in human and monkey. J Neurosci 21:161-165.
17.
Elston GN, Benavides-Piccione R, Elston A, DeFelipe J, Manger PR (2005a): Pyramidal cell specialization in the occipitotemporal cortex of the Chacma baboon (Papio ursinus). Exp Brain Res 167:496-503.
18.
Elston GN, Benavides-Piccione R, Elston A, Manger PR, DeFelipe J (2005b): Pyramidal cell specialization in the occipitotemporal cortex of the vervet monkey (Cercopithecus pygerythrus). Neuroreport 16:967-970.
19.
Elston GN, Benavides-Piccione R, Elston A, Manger PR, DeFelipe J (2011): Pyramidal cells in the prefrontal cortex: comparative observations reveal unparalleled specializations in neuronal structure among primate species. Front Neuroanat 5:2.
20.
Elston GN, Benavides-Piccione R, Elston A, Zietsch B, DeFelipe J, Manger PR, Casagrande V, Kaas JH (2006): Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. Anat Rec A Discov Mol Cel Evol Biol 288A:26-35.
21.
Elston GN, Elston A, Casagrande VA, Kaas JH (2005d): Pyramidal neurons of granular prefrontal cortex of the galago: complexity in the evolution of the psychic cell. Anat Rec A Discov Mol Cel Evol Biol 285:610-618.
22.
Elston GN, Elston A, Kaas JH, Casagrande VA (2005c): Regional specialization in pyramidal cell structure in the visual cortex of the galago: an intracellular injection study with comparative notes on new world and old world monkeys. Brain Behav Evol 66:10-21.
23.
Elston GN, Rosa MG (1998): Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cereb Cortex 8:278-294.
24.
Elston GN, Rosa MG, Calford MB (1996): Comparison of the dendritic fields of layer III pyramidal neurones in striate and extrastriate visual areas of the marmoset: a Lucifer yellow intracellular injection study. Cereb Cortex 6:807-813.
25.
Elston GN, Tweedale R, Rosa MG (1999): Cellular heterogeneity in cerebral cortex: a study of the morphology of pyramidal neurones in visual areas of the marmoset monkey. J Comp Neurol 415:33-51.
26.
Finlay BL, Darlington RB (1995): Linked regularities in the development and evolution of mammalian brains. Science 268:1578-1584.
27.
Finlay BL, Darlington RB, Nicastro N (2001): Developmental structure in brain evolution. Behav Brain Sci 24:263-308.
28.
Fonesca-Azevedo K, Herculano-Houzel S (2012): Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution. Proc Natl Acad Sci USA 109:18571-18576.
29.
Gould SJ (2000): The Structure of Evolutionary Theory. Cambridge, Belknap Press.
30.
Gravett N, Bhagwandin A, Fuxe K, Manger PR (2009): Nuclear organization and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the rock hyrax, Procavia capensis. J Chem Neuroanat 38:57-74.
31.
Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM (2009): Von Economo neurons in the elephant brain. Anat Rec 292:242-248.
32.
Herculano-Houzel S (2012): Neuronal scaling rules for primate brains: the primate advantage. Prog Brain Res 195:325-340.
33.
Higdon JW, Bininda-Emonds OR, Beck RM, Ferguson SH (2007): Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset. BMC Evol Biol 7:216.
34.
Holloway RL (1968): The evolution of the primate brain: some aspects of quantitative relations. Brain Res 7:121-172.
35.
Jacobs B, Lubs K, Hannan M, Anderson K, Butti C, Sherwood CC, Hof PR, Manger PR (2011): Neuronal morphology in the African elephant (Loxodonta africana) neocortex. Brain Struct Funct 215:273-298.
36.
Jerison HJ (1973): Evolution of the Brain and Intelligence. New York, Academic Press.
37.
Manger PR (2005): Establishing order at the systems level in mammalian brain evolution. Brain Res Bull 66:282-289.
38.
Manger PR (2006): An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol Rev 81:293-338.
39.
Manger PR, Hemingway J, Spocter MA, Gallagher A (2012a): The mass of the human brain: is it a spandrel?; in Reynolds S, Gallagher A (eds): African Genesis, Perspectives on Hominin Evolution. Cambridge, Cambridge University Press, pp 181-204.
40.
Manger PR, Pillay P, Maseko BC, Bhagwandin A, Gravett N, Moon DJ, Jillani NE, Hemingway J (2009): Acquisition of brains from the African elephant (Loxodonta africana): perfusion-fixation and dissection. J Neurosci Meth 179:16-21.
41.
Manger PR, Prowse M, Haagensen M, Hemingway J (2012b): A quantitative analysis of neocortical gyrencephaly in African elephants (Loxodonta africana) and six species of cetaceans: comparison to other mammals. J Comp Neurol 520:2430-2439.
42.
Marino L (2002): Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav Evol 59:21-32.
43.
Marino L, Butti C, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Lusseau D, McCowan B, Nimchinsky EA, Pack AA, Reidenberg JS, Reiss D, Rendell L, Uhen MD, Van der Gucht E, Whitehead H (2008): A claim in search of evidence: reply to Manger's thermogenesis hypothesis of cetacean brain structure. Biol Rev 83:417-440.
44.
Maseko BC, Jacobs B, Spocter MA, Sherwood CC, Hof PR, Manger PR (2013a): Qualitative and quantitative aspects of the microanatomy of the African elephant cerebellar cortex. Brain Behav Evol 81:40-55.
45.
Maseko BC, Patzke N, Fuxe K, Manger PR (2013b): Architectural organization of the African elephant diencephalon and brainstem. Brain Behav Evol, in press.
46.
Maseko BC, Spocter MA, Haagensen M, Manger PR (2012): Elephants have relatively the largest cerebellum size of mammals. Anat Rec 295:661-672.
47.
Maynard Smith J (1988): Did Darwin Get It Right? Essays on Games, Sex and Evolution. London, Penguin Books.
48.
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex. Ann Rev Neurosci 24:167-202.
49.
Poirazi P, Mel BW (2001): Impact of active dendrites and structural plasticity on the storage capacity of neural tissue. Neuron 29:779-796.
50.
Price SA, Bininda-Emonds OR, Gittleman JL (2005): A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biol Rev 80:445-473.
51.
Sanders WJ, Gheerbrandt E, Harris JM, Saegusa H, Delmer C (2010): Proboscidea; in Werdelin L, Sanders WJ (eds): Cenozoic Mammals of Africa. Los Angeles, University of California Press, pp 161-252.
52.
Shoshani J, Kupsky WJ, Marchant GH (2006): Elephant brain. 1. Gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124-157.
53.
Spruston N (2008): Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206-221.
54.
Szelényi Z (1998): Neuroglia: possible role in thermogenesis and body temperature control. Med Hypotheses 50:191-197.
55.
Tattersall I, Schwartz JH (2001): Extinct Humans. New York, Westview Press.
56.
von Bonin G (1937): Brain-weight and body-weight in mammals. J Gen Psych 16:379-389.
57.
Wood B, Collard M (1999): The changing face of genus Homo. Evol Anthropol 8:195-207.
58.
Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001): Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686-693.
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