title: Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution.
abstract: Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.
authors.affiliation: Department of Anthropology, University College London, 14 Taviton Street, London WC1H 0BW, UK. wojtek.przepiorka@sociology.ox.ac.uk
authors.forename: J B
authors.initials: JB
authors.lastname: Smaers
authors.forename: C
authors.initials: C
authors.lastname: Soligo
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002531:Cerebellum / Q000033:anatomy & histology*; D005260:Female; D000882:Haplorhini / Q000033:anatomy & histology*; D008297:Male; D009044:Motor Cortex / Q000033:anatomy & histology*; D015999:Multivariate Analysis; D010802:Phylogeny; D017397:Prefrontal Cortex / Q000033:anatomy & histology*; D011323:Primates; D025341:Principal Component Analysis
references.citation: Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21582-6
references.pmid: 21098277
references.citation: BMC Biol. 2010 Jan 27;8:9
references.pmid: 20105283
references.citation: Evolution. 2009 Dec;63(12):3258-68
references.pmid: 19663993
references.citation: J Neurosci. 2001 Jan 15;21(2):700-12
references.pmid: 11160449
references.citation: Behav Brain Sci. 2001 Apr;24(2):263-78; discussion 278-308
references.pmid: 11530543
references.citation: Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3562-7
references.pmid: 17360682
references.citation: J Physiol. 1969 Jun;202(2):437-70
references.pmid: 5784296
references.citation: Am Nat. 2008 Jul;172 Suppl 1:S63-71
references.pmid: 18554145
references.citation: Folia Primatol (Basel). 1981;35(1):1-29
references.pmid: 7014398
references.citation: PLoS One. 2010 Feb 09;5(2):e9123
references.pmid: 20161758
references.citation: Neuropsychologia. 2010 Oct;48(12):3554-62
references.pmid: 20713074
references.citation: Neuroimage. 2012 Jan 2;59(1):582-600
references.pmid: 21840405
references.citation: Cereb Cortex. 2002 Sep;12(9):926-35
references.pmid: 12183392
references.citation: PLoS One. 2011 Apr 06;6(4):e18277
references.pmid: 21494328
references.citation: Science. 1960 Sep 9;132(3428):670-2
references.pmid: 13835142
references.citation: Biol Lett. 2005 Sep 22;1(3):283-6
references.pmid: 17148188
references.citation: Proc Biol Sci. 1993 Nov 22;254(1340):75-82
references.pmid: 8290611
references.citation: Brain Behav Evol. 2012;79(3):205-12
references.pmid: 22327843
references.citation: Nature. 2000 Jun 29;405(6790):1055-8
references.pmid: 10890446
references.citation: Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16044-9
references.pmid: 21896760
references.citation: Brain Res Brain Res Rev. 2000 Mar;31(2-3):236-50
references.pmid: 10719151
references.citation: Annu Rev Neurosci. 2010;33:299-324
references.pmid: 20350167
references.citation: Annu Rev Neurosci. 2002;25:563-93
references.pmid: 12052921
references.citation: Science. 1996 Sep 6;273(5280):1399-402
references.pmid: 8703077
references.citation: Syst Biol. 2011 Jan;60(1):16-31
references.pmid: 21051775
references.citation: Exp Brain Res. 1997 Jun;115(1):1-5
references.pmid: 9224828
references.citation: Nat Rev Neurosci. 2007 Sep;8(9):657-61
references.pmid: 17700624
references.citation: J Hum Evol. 2003 Jan;44(1):3-10
references.pmid: 12604300
references.citation: Brain Behav Evol. 2011;77(2):67-78
references.pmid: 21335939
references.citation: Brain Behav Evol. 2010;76(1):32-44
references.pmid: 20926854
references.citation: J Neurosci. 2003 Sep 10;23(23):8432-44
references.pmid: 12968006
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Aug 5;367(1599):2097-107
references.pmid: 22734053
references.citation: Ann N Y Acad Sci. 2011 May;1225 Suppl 1:E94-104
references.pmid: 21599701
references.citation: J Comp Neurol. 2012 Sep 1;520(13):2917-29
references.pmid: 22350926
references.citation: Neuroimage. 2009 Jan 15;44(2):489-501
references.pmid: 18835452
references.citation: J Neurophysiol. 2011 Nov;106(5):2322-45
references.pmid: 21795627
references.citation: Brain Sci. 2012 May 18;2(2):203-24
references.pmid: 24962772
references.citation: Science. 2007 Sep 7;317(5843):1344-7
references.pmid: 17823343
references.citation: Neurosci Lett. 1995 Oct 27;199(3):175-8
references.pmid: 8577391
references.citation: Prog Brain Res. 2012;195:393-412
references.pmid: 22230638
references.citation: Science. 2010 Sep 17;329(5998):1541-3
references.pmid: 20847276
references.citation: Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4436-41
references.pmid: 11891325
references.citation: Brain Behav Evol. 2007;70(2):115-24
references.pmid: 17510549
references.citation: J Neurosci. 2005 Apr 27;25(17):4270-8
references.pmid: 15858053
references.citation: Behav Brain Res. 2009 Apr 12;199(1):61-75
references.pmid: 19061920
references.citation: J Comp Neurol. 2007 Jan 10;500(2):211-21
references.pmid: 17111358
references.citation: Curr Biol. 2006 Nov 7;16(21):R910-4
references.pmid: 17084684
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5460-5
references.pmid: 15784743
references.citation: Proc Natl Acad Sci U S A. 2000 May 9;97(10):5621-6
references.pmid: 10792049
references.citation: Prog Brain Res. 1991;87:307-421
references.pmid: 1678191
references.citation: Ann N Y Acad Sci. 2011 Apr;1225:176-90
references.pmid: 21535004
references.citation: Nat Neurosci. 2010 Apr;13(4):507-12
references.pmid: 20208526
references.citation: Cortex. 2011 Jan;47(1):59-80
references.pmid: 19833328
references.citation: J Evol Biol. 2012 May;25(5):981-94
references.pmid: 22435703
references.citation: Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):4196-201
references.pmid: 11274442
references.citation: Ann N Y Acad Sci. 2013 Jun;1288:59-69
references.pmid: 23647442
references.citation: Brain Behav Evol. 1997;50(3):167-82
references.pmid: 9288416
references.citation: Nat Rev Neurosci. 2000 Oct;1(1):59-65
references.pmid: 11252769
references.citation: Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18006-11
references.pmid: 23071335
references.citation: Cereb Cortex. 2009 Oct;19(10):2485-97
references.pmid: 19592571
references.citation: Nature. 2001 Feb 8;409(6821):710-4
references.pmid: 11217859
references.citation: Science. 1995 Jun 16;268(5217):1578-84
references.pmid: 7777856
references.citation: J Neurosci. 2010 Oct 13;30(41):13906-15
references.pmid: 20943931
references.citation: PLoS Comput Biol. 2010 Jun 10;6(6):e1000808
references.pmid: 20548945