title: Evolutionary and developmental implications of asymmetric brain folding in a large primate pedigree.
abstract: Bilateral symmetry is a fundamental property of the vertebrate central nervous system. Local deviations from symmetry provide various types of information about the development, evolution, and function of elements within the CNS, especially the cerebral hemispheres. Here, we quantify the pattern and extent of asymmetry in cortical folding within the cerebrum of Papio baboons and assess the evolutionary and developmental implications of the findings. Analyses of directional asymmetry show a population-level trend in length measurements indicating that baboons are genetically predisposed to be asymmetrical, with the right side longer than the left in the anterior cerebrum while the left side is longer than the right posteriorly. We also find a corresponding bias to display a right frontal petalia (overgrowth of the anterior pole of the cerebral cortex on the right side). By quantifying fluctuating asymmetry, we assess canalization of brain features and the susceptibility of the baboon brain to developmental perturbations. We find that features are differentially canalized depending on their ontogenetic timing. We further deduce that development of the two hemispheres is to some degree independent. This independence has important implications for the evolution of cerebral hemispheres and their separate specialization. Asymmetry is a major feature of primate brains and is characteristic of both brain structure and function.
authors.affiliation: Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri, 63110. Elizabeth.Atkinson@stonybrook.edu.|Current Address: Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, 11794. Elizabeth.Atkinson@stonybrook.edu.
authors.forename: Elizabeth G
authors.initials: EG
authors.lastname: Atkinson
authors.affiliation: Human Genome Sequencing Center and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas, 77030.
authors.forename: Jeffrey
authors.initials: J
authors.lastname: Rogers
authors.affiliation: Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri, 63110.
authors.forename: James M
authors.initials: JM
authors.lastname: Cheverud
mesh_terms: D000818:Animals; D005075:Biological Evolution; D054022:Cerebrum / Q000033:anatomy & histology* / Q000502:physiology*; D005260:Female; D008297:Male; D010375:Pedigree; D011323:Primates / Q000033:anatomy & histology* / Q000502:physiology*
keywords: Baboon; developmental noise; gyrification; morphological integration; primate brain evolution
references.citation: Evolution. 1998 Oct;52(5):1363-1375
references.pmid: 28565401
references.citation: Neuropsychologia. 2007 Jun 11;45(10):2398-401
references.pmid: 17418285
references.citation: Brain Struct Funct. 2014 Nov;219(6):2187-94
references.pmid: 23928747
references.citation: Trends Neurosci. 2013 May;36(5):275-84
references.pmid: 23415112
references.citation: Neuroimage. 2010 Nov 15;53(3):1126-34
references.pmid: 20035879
references.citation: Wiley Interdiscip Rev Cogn Sci. 2012 Jan;3(1):1-17
references.pmid: 26302469
references.citation: Front Evol Neurosci. 2012 Jan 03;3:11
references.pmid: 22319495
references.citation: Hum Brain Mapp. 2007 Jun;28(6):576-83
references.pmid: 17437285
references.citation: Behav Neurosci. 2011 Aug;125(4):653-60
references.pmid: 21534647
references.citation: Neuropsychologia. 2006;44(12):2582-6
references.pmid: 16730360
references.citation: PLoS One. 2011;6(12):e28243
references.pmid: 22205941
references.citation: Proc Natl Acad Sci U S A. 2005 Aug 30;102(35):12634-8
references.pmid: 16105943
references.citation: Nat Commun. 2014 Jul 22;5:4469
references.pmid: 25047085
references.citation: Am J Phys Anthropol. 2013 Jan;150(1):133-40
references.pmid: 23180628
references.citation: J Anthropol Sci. 2008;86:7-35
references.pmid: 19934467
references.citation: J Hered. 1990 Jan-Feb;81(1):51-7
references.pmid: 2332614
references.citation: Philos Trans R Soc Lond B Biol Sci. 2009 Apr 12;364(1519):867-79
references.pmid: 19064358
references.citation: Brain Res. 1990 Oct 15;530(1):40-8
references.pmid: 2271951
references.citation: J Hered. 1995 Jul-Aug;86(4):280-8
references.pmid: 7657996
references.citation: Cortex. 2012 Jan;48(1):82-96
references.pmid: 22088488
references.citation: Neuropsychologia. 1990;28(6):529-46
references.pmid: 2203994
references.citation: Neuroimage. 2008 Aug 15;42(2):491-7
references.pmid: 18586523
references.citation: J Comp Neurol. 2008 Sep 1;510(1):117-28
references.pmid: 18612968
references.citation: Brain Behav Evol. 2001 Feb;57(2):98-105
references.pmid: 11435670
references.citation: Psychon Bull Rev. 1996 Dec;3(4):449-57
references.pmid: 24213978
references.citation: Evolution. 1982 May;36(3):499-516
references.pmid: 28568050
references.citation: Genetics. 2015 Jun;200(2):651-65
references.pmid: 25873632
references.citation: Evolution. 1998 Jun;52(3):647-656
references.pmid: 28565257
references.citation: Cereb Cortex. 2010 Mar;20(3):730-42
references.pmid: 19620620
references.citation: J Neurosci. 2009 Nov 18;29(46):14607-16
references.pmid: 19923293
references.citation: Neuropsychologia. 2000;38(4):493-9
references.pmid: 10683399
references.citation: Behav Neurosci. 2000 Aug;114(4):739-48
references.pmid: 10959533
references.citation: Cereb Cortex. 1994 Jul-Aug;4(4):331-43
references.pmid: 7950307
references.citation: J Hum Evol. 2010 Jul;59(1):54-69
references.pmid: 20537369
references.citation: Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11163-70
references.pmid: 20484679
references.citation: Front Hum Neurosci. 2009 Nov 09;3:31
references.pmid: 19915731
references.citation: Psychol Bull. 2006 Jul;132(4):538-59
references.pmid: 16822166
references.citation: Curr Opin Neurobiol. 2014 Oct;28:10-4
references.pmid: 24835547
references.citation: Neuropsychologia. 2011 Jun;49(7):2004-12
references.pmid: 21447349
references.citation: Nat Rev Neurosci. 2006 Aug;7(8):655-62
references.pmid: 16858393
references.citation: Evolution. 2010 Oct;64(10):2935-51
references.pmid: 20482613
references.citation: Brain Behav Evol. 2001 Jun;57(6):349-58
references.pmid: 11713389
references.citation: J Comp Neurol. 2007 Mar 10;501(2):243-59
references.pmid: 17226764
references.citation: Brain Res Rev. 2011 Jun 24;67(1-2):56-72
references.pmid: 21059373
references.citation: Brain Lang. 2009 Mar;108(3):167-74
references.pmid: 19091390
references.citation: J Hum Evol. 2011 May;60(5):605-11
references.pmid: 21334723
references.citation: Nat Neurosci. 2001 Dec;4(12):1253-8
references.pmid: 11694885
references.citation: PLoS One. 2011;7(1):e29581
references.pmid: 22242147
references.citation: Behav Neurosci. 2004 Dec;118(6):1176-83
references.pmid: 15598127
references.citation: J Hum Evol. 1999 Aug;37(2):191-223
references.pmid: 10444351
references.citation: Brain Behav Evol. 2000 Jan;55(1):37-43
references.pmid: 10773624
references.citation: Cereb Cortex. 2010 Mar;20(3):602-11
references.pmid: 19561060
references.citation: Cortex. 2015 Jun;67:30-6
references.pmid: 25863470
references.citation: Am J Phys Anthropol. 1984 Aug;64(4):401-11
references.pmid: 6486247
references.citation: Anat Rec A Discov Mol Cell Evol Biol. 2006 Aug;288(8):867-76
references.pmid: 16835937
references.citation: Neuroimage. 2012 Jul 2;61(3):533-41
references.pmid: 22504765
references.citation: Anat Rec (Hoboken). 2012 Jul;295(7):1065-74
references.pmid: 22593081