The evolution of brain size among the Homininae and selection at ASPM and MCPH1 genes
DOI:
https://doi.org/10.37819/biosis.002.02.0104Keywords:
Brain size, Homo, Microcephaly-associated genes, Molecular evolution, Natural selectionAbstract
We examined the evolutionary relationship of the ASPM (abnormal spindle-like microcephaly associated) and MCPH1 (microcephalin-1) genes with brain volume among humans and other primates. We obtained sequences of these genes from 14 simiiform species including hominins. Two phylogenetic analyses of ASPM exon 3 and MCPH1 exons 8 and 11 were performed to maximize taxon sampling or sequence extension to compare the nucleotide substitution and encephalization rates, and examine signals of selection. Further assessment of selection among humans was done through the analysis of non-synonymous and synonymous substitutions (dN/dS), and linkage disequilibrium (LD) patterns. We found that the accelerated evolution of brain size in hominids, is related to synchronic acceleration in the substitution rates of ASPM and MCPH1, and to signals of positive selection, especially in hominins. The dN/dS and LD analyses in Homo detected sites under positive selection and some regions with haplotype blocks at several candidate sites surrounded by blocks in LD-equilibrium. Accelerations and signals of positive selection in ASPM and MCPH1 occurred in different lineages and periods being ASPM more closely related with the brain evolution of hominins. MCPH1 evolved under positive selection in different lineages of the Catarrhini, suggesting independent evolutionary roles of this gene among primates.
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Akey JM. 2009. Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Res. 19(5), 711–722. htps://doi.org/10.1101/gr.086652.108
Ali F, Meier R. 2008. Positive selection in ASPM is correlated with cerebral cortex evolution across primates but not with whole-brain size. Mol. Biol. Evol. 25(11), 2247–2250. https://doi.org/10.1093/molbev/msn184
Allman J, McLaughlin T, Hakeem A. 1993. Brain weight and life-span in primate species. Proc. Natl. Acad. Sci. USA 90(1):118–122. https://doi.org/10.1073/pnas.90.1.118
Anisimova M, Bielawski JP, Yang Z. 2001. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol. Biol. Evol. 18(8):1585–1592. https://doi.org/10.1093/oxfordjournals.molbev.a003945
Arroyo M, Kuriyama R, Trimborn M, Keifenheim D, Cañuelo A, Sánchez A. 2017. MCPH1, mutated in primary microcephaly, is required for efficient chromosome alignment during mitosis. Sci. Rep. 7:13019. https://doi.org/10.1038/s41598-017-12793-7
Auton A, Abecasis GR, Altshuler DM, Durbin RM, Bentley DR, Chakravarti A, Schloss JA. 2015. A global reference for human genetic variation. Nature 526(7571):68–74. https://doi.org/10.1038/nature15393
Bond J, Roberts E, Mochida GH, Hampshire DJ, Scott S, Askham JM, Springell K, Mahadevan M, Crow YJ, Markham AF, et al. 2002. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32(2):316–320. https://doi.org/10.1038/ng995
Bond J, Woods CG. 2006. Cytoskeletal genes regulating brain size. Curr. Opin. Cell Biol. 18(1):95–101. https://doi.org/10.1016/j.ceb.2005.11.004
Borries C, Koenig A, Winkler P. 2001. Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behav. Ecol. Sociobiol. 50(5), 391–402. https://doi.org/10.1007/s002650100391
Bush GL, Case SM, Wilson AC, Patton JL. 1977. Rapid speciation and chromosomal evolution in mammals. Proc. Natl. Acad. Sci. USA 74(9), 3942–3946. https://doi.org/10.1073/pnas.74.9.3942
Charlesworth B. 2009. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10(3):195–205. https://doi.org/10.1038/nrg2526
Deacon TW. 1997. The symbolic species: the co-evolution of language and the brain. New York (NY): W.W. Norton & Co.
Delson E. 1992. Evolution of old word monkeys. In: Jones JS, Martin RD, Pilbeam D, Bunney S, editors. The Cambridge Encyclopedia of Human Evolution. Cambridge (UK): Cambridge University Press; p. 217–222.
Depaulis F, Veuille M. 1998. Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol. Biol. Evol. 15(12):1788–1790. https://doi.org/10.1093/oxfordjournals.molbev.a025905
Desir J, Cassart M, David P, Van Bogaert P, Abramowicz M. 2008. Primary microcephaly with ASPM mutation shows simplified cortical gyration with antero‐posterior gradient pre‐ and post‐natally. Am. J. Med. Genet. Part A 146A:1439–1443. https://doi.org/10.1002/ajmg.a.32312
Dorus S, Vallender EJ, Evans PD, Anderson JR, Gilbert S, Mahowald M, Lahn BT. 2004. Accelerated Evolution of Nervous System Genes in the Origin of Homo sapiens. Cell 119(7):1027–1040. https://doi.org/10.1016/j.cell.2004.11.040
Evans PD, Anderson JR, Vallender EJ, Gilbert SL, Malcolm CM, Dorus S, Lahn BT. 2004. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum. Mol. Genet. 13(5):489–494. https://doi.org/10.1093/hmg/ddh055
Evans PD, Gilbert SL, Mekel-Bobrov N, Vallender EJ, Anderson JR, Vaez-Azizi LM, Tishkoff SA, Hudson RR, Lahn BT. 2005. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309(5741):1717–1720. https://doi.org/10.1126/science.1113722
Evans PD, Mekel-bobrov N, Vallender EJ, Hudson RR, Lahn BT. 2006. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc. Natl. Acad. Sci. USA 103(48):18178–18183. https://doi.org/10.1073/pnas.0606966103
Falk D. 1983. Cerebral Cortices of East African Early Hominids. Science 221(4615):1072–1074.
Fish JL, Kosodo Y, Enard W, Pääbo S, Huttner WB. 2006. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl. Acad. Sci. USA 103(27):10438–10443. https://doi.org/10.1073/pnas.0604066103
Gaskin DE. 1982. The ecology of whales and dolphins. London: Heineman.
Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. 2001. Teeth, Brains, and Primate Life Histories. Am. J. Phys. Anthropol. 114:192–214. https://doi.org/10.1002/1096-8644(200103)114:3%3C192::AID-AJPA1020%3E3.0.CO;2-Q
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MHY, et al. 2010. A draft sequence of the Neandertal genome. Science 328(5979):710–722. https://doi.org/10.1126/science.1188021
Hajdinjak M, Fu Q, Hübner A, Petr M, Mafessoni F, Grote S, Skoglund P, Narasimham V, Rougier H, Crevecoeur I, et al. 2018. Reconstructing the genetic history of late Neanderthals. Nature 555:652–656. https://doi.org/10.1038/nature26151
Hartwig W, Rosenberger AI, Norconk MA, Owl MY. 2011. Relative Brain Size, Gut Size, and Evolution in New World Monkeys. Anat. Rec. 294:2207–2221. https://doi.org/10.1002/ar.21515
Haygood R, Fedrigo O, Hanson B, Yokoyama K, Wray GA. 2007. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat. Genet. 39(9):1140–1144. https://doi.org/10.1038/npre.2007.69.1
Hoekstra HE, Coyne J. 2007. The locus of evolution: Evo Devo and the genetics of adaptation. Evolution 61(5): 995–1016. https://doi.org/10.1111/j.1558-5646.2007.00105.x
Holloway RL, Clarke RJ, Tobias PV. 2004. Posterior lunate sulcus in Australopithecus africanus: was Dart right? Hum. Palaeontol. Prehist. 3:287–293. https://doi.org/10.1016/j.crpv.2003.09.030
Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755.
Isler K, Kirk EC, Miller JMA, Albrecht GA, Gelvin BR Martin RD 2008. Endocranial volumes of primate species: Scaling analyses using a comprehensive and reliable dataset. J. Hum. Evol. 55(6): 967–987. https://doi.org/10.1016/j.jhevol.2008.08.004
Jackson A, Eastwood H, Bell S, Adu J, Toomes C, Carr I, Roberts E, Hampshire D, Crow Y, Mighell A, et al. 2002 Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71:136–142. https://doi.org/10.1086/341283
Jacobs GS, Sluckin TJ, Kivisild T. 2016. Refining the use of linkage disequilibrium as a robust signature of selective sweeps. Genetics 203(4):1807–1825. https://doi.org/10.1093/genetics/203.4.NP
Jerison HJ. 1973. Evolution of the brain and intelligence. New York (NY): Academic Press.
Jones JS, Martin RD, Pilbeam D, Bunney S, editors. The Cambridge Encyclopedia of Human Evolution. Cambridge (UK): Cambridge University Press.
Kelley JL, Madeoy J, Calhoun JC, Swanson W, Akey JM. 2006. Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Res. 16(8):980–989. https://doi.org/10.1101/gr.5157306
Kelly JK. 1997. A test of neutrality based on interlocus associations. Genetics 146(3):1197–1206.
Kim Y, Nielsen R. 2004. Linkage disequilibrium as a signature of selective sweeps. Genetics 167(3):1513–1524. https://doi.org/10.1534/genetics.103.025387
Ko KH. 2016. Hominin interbreeding and the evolution of human variation. J. Biol. Res.-Thessaloniki 23(1):17. https://doi.org/10.1186/s40709-016-0054-7
Kouprina N, Pavlicek A, Mochida GH, Solomon G, Gersch W, Yoon YH, Collura R, Ruvolo M, Barrett JC, Woods CG, et al. 2004. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biology, 2(5), 653–663. 2004. https://doi.org/10.1371/journal.pbio.0020126
Kronenberg ZN, Fiddes IT, Gordon D, Murali S, Cantsilieris S, Meyerson OS, Underwood JG, Nelson BJ, Chaisson MJP, Dougherty ML, et al. 2018. High-resolution comparative analysis of great ape genomes. Science 360(1085): eaar6343. https://doi.org/10.1126/science.aar6343
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
LeMaho Y, Goffart M, Rochas A, Felbabel H, Chatonnet J. 1981. Thermoregulation in the only nocturnal simian: the night monkey Aotus trivirgatus. Am. J. Physiol. 240(3):R156–R165. https://doi.org/10.1152/ajpregu.1981.240.3.R156
Leyva Hernández S. 2016. Genes implicados en la determinación del volumen cerebral en el linaje humano [bachelor’s tesis]. Ciudad de México: Escuela Nacional de Antropología e Historia.
Lieberman D. 2011 The evolution of the human head. Cambridge (MA): Belknap Press of Harvard University Press.
Lin S, Rai R, Li K, Xu Z, Elledge SJ. 2005. BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1–Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl. Acad. Sci. USA 102(42):15105–15109. https://doi.org/10.1073/pnas.0507722102
Maddison DR, Maddison WP. 2003. MacClade 4. ver. 4.06. Sunderland (MA): Sinauer.
Marino L. 2002. Brain size evolution. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press; p. 158-162.
Martin RD. 1996. Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol. Sci. 11:149–156. https://doi.org/10.1152/physiologyonline.1996.11.4.149
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26(19):2462–2463. https://doi.org/10.1093/bioinformatics/btq467
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. 2015. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 1(1):1–5. https://doi.org/10.1093/ve/vev003
Martin D, Rybicki E. 2000. RDP: Detection of recombination amongst aligned sequences. Bioinformatics 16(6):562–563. https://doi.org/10.1093/bioinformatics/16.6.562
McDaniel MA. 2005. Big-brained people are smarter: A meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence 33(4): 337–346. https://doi.org/10.1016/j.intell.2004.11.005
McHenry HM 1994. Tempo and mode in human evolution. Proc. Natl. Acad. Sci. USA 91(15):6780–6786.
Medrano González L. 2009. La evolución de los cetáceos. In: Morrone JJ, Magaña P, editors. Evolución biológica. Una visión actualizada desde la revista Ciencias. Ciudad de México: Facultad de Ciencias, Universidad Nacional Autónoma de México; p. 539–588.
Meyer M, Kircher M, Gansauge MT,1 Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prüfer K, Filippo C, et al. 2012. A High-Coverage Genome Sequence from an Archaic Denisovan Individual. Science, 222(2012):1–14. https://doi.org/10.1126/science.1224344
Miyashita N Langley CH. 1988. Molecular and Phenotypic Variation of the white Locus Region in Drosophila melanogaster. Genetics 120:199–212.
Montgomery SH, Capellini I, Venditti C, Barton RA, Mundy NI. 2011. Adaptive evolution of four microcephaly genes and the evolution of brain size in anthropoid primates. Mol. Biol. Evol. 28(1):625–638. https://doi.org/10.1093/molbev/msq237
Montgomery SH, Mundy NI. 2010. Brain evolution: Microcephaly genes weigh in. Curr. Biol. 20(5):R244–R246. https://doi.org/10.1016/j.cub.2010.01.043
Muthukrishna M, Doebeli M, Chudek M, Henrich J. 2018. The Cultural Brain Hypothesis: How culture drives brain expansion, sociality, and life history. PLoS Comput. Biol. 14(11): 1–37. https://doi.org/10.1371/journal.pcbi.1006504
Nei M, Suzuki Y, Nozawa M. 2010. The neutral theory of molecular evolution in the genomic era. Annu. Rev. Genom. Hum. G. 11(1):265–289. https://doi.org/10.1146/annurev-genom-082908-150129
Neubauer S, Hublin J. 2012. The evolution of human brain development. Evol. Biol. 39:568–586.
Neubauer S, Hublin JJ, Gunz P. 2018. The evolution of modern human brain shape. Sci. Adv. 4(1): eaao5961. https://doi.org/10.1126/sciadv.aao5961
Padidam M, Sawyer S, Fauquet CM. 1999. Possible emergence of new geminiviruses by frequent recombination. Virology 265(2):218–225. https://doi.org/10.1006/viro.1999.0056
Page SL, Chiu C, Goodman M. 1999. Molecular Phylogeny of Old World Monkeys (Cercopithecidae) as Inferred from -Globin DNA Sequences. Mol. Phyl. Evol. 13(2):348–359. https://doi.org/10.1006/mpev.1999.0653
Paixão-Côrtes VR, Viscardi LH, Salzano FM, Hünemeier T, Bortolini MC. 2012. Homo sapiens, Homo neanderthalensis and the Denisova specimen: New insights on their evolutionary histories using whole-genome comparisons. Genet. Mol. Biol. 35(4 supl.1):904–911. https://doi.org/10.1590/S1415-47572012000600003
Passemard S, Verloes A, de Villemeur TB, Boespflug-Tanguy O, Hernandez K, Laurent M, Isidor B, Alberti C, Pouvreau N, Drunat S, et al. 2016. Abnormal spindle-like microcephaly-associated (ASPM) mutations strongly disrupt neocortical structure but spare the hippocampus and long-term memory. Cortex 74:158–176. https://doi.org/10.1016/j.cortex.2015.10.010
Pennings PS, Hermisson J. 2006. Soft sweeps III: The signature of positive selection from recurrent mutation. PLoS Genet. 2(12): e186. https://doi.org/10.1371/journal.pgen.0020186
Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MAM, Kessing B, Pontius J, Roelke M, Rumpler Y, Schneider MPC, Silva A, O’Brien SJ, Pecon-Slattery J. 2011. A Molecular Phylogeny of Living Primates. PLoS Genet. 7(3): e1001342. https://doi.org/10.1371/journal.pgen.1001342
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera--a visualization system for exploratory research and analysis. J. Comput. Chem. 25(13):1605-1612. https://doi.org/10.1002/jcc.20084
Ponting C, Jackson AP. 2005. Evolution of primary microcephaly genes and the enlargement of primate brains. Science 14(3):241–248. https://doi.org/10.1016/j.gde.2005.04.009
Pontzer H, Raichlen AC, Gordon AD, Schroepfer-Walker KK, Hare B, O’Neill MC, Muldoon KM, Dunsworth HM, Wood BM, Isler K, et al. 2014. Primate energy expenditure and life history. Proc. Natl. Acad. Sci. USA 111(4):1433–1437. https://doi.org/10.1073/pnas.1316940111
Posthuma D, Baaré WFC, Pol HEH, Kahn RS, Boomsma DI, De Geus EJC. 2003. Genetic Correlations Between Brain Volumes and the WAIS-III Dimensions of Verbal Comprehension, Working Memory, Perceptual Organization, and Processing Speed. Twin Res. 6(2):131–139. https://doi.org/10.1375/twin.6.2.131
Prüfer K, de Filippo C, Grote S, Mafessoni F, Korlevi P, Hajdinjak M, Vernot B, Skov L, Hsieh P, Peyrégne S, et al. 2017. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358(6363):655–658. https://doi.org/10.1126/science.aao1887
Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C, et al. 2014. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature, 505(7481):43–49. https://doi.org/10.1038/nature12886
Pulvers JN, Bryk J, Fish JL, Wilsch-Bräuninger M, Arai Y, Schreier D, Naumann R, Helppi J, Habermann B, Vogt J, et al. 2010. Mutations in mouse ASPM (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline. Proc. Natl. Acad. Sci. USA 107(38):16595–16600. https://doi.org/10.1073/pnas.1010494107
Ramos-Onsins SE, Rozas J. 2001. Statistical Properties of New Neutrality Tests Against Population Growth. Mol. Biol. Evol. 19(12):2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Rightmire GP. 1998. Human evolution in the Middle Pleistocene: the role of Homo heidelbergensis. Evol. Anthropol. 6(6):218–227. https://doi.org/10.1002/(SICI)1520-6505(1998)6:6%3C218::AID-EVAN4%3E3.0.CO;2-6
Rightmire GP. 2004. Brain size and encephalization in early to mid-Pleistocene Homo. Am. J. Phys. Anthropol. 124(2):109–123. https://doi.org/10.1002/ajpa.10346
Robson SL, Wood B. 2008. Hominin life history: reconstruction and evolution. J. Anat. 212(4):394–425. https://doi.org/10.1111/j.1469-7580.2008.00867.x
Ross C. 1992. Basal Metabolic Rate, Body Weight and Diet in Primates: An Evaluation of the Evidence. Folia Primatol. 58(1):7–23. https://doi.org/10.1159/000156602
Roth G, Dicke U. 2012. Evolution of the brain and intelligence in primates. In: Hofman MA, Falk D, editors. Prog. Brain Res. 195:413–30.
Rozas J, Gullaud M, Blandin G, Aguadé M. 2001. DNA variation at the rp49 gene region of Drosophila simulans: evolutionary inferences from an unusual haplotype structure. Genetics 158(3):1147–1155. https://doi.org/10.1093/genetics/158.3.1147
Rozas J, Rozas R. 1999. DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15(2): 174–175. https://doi.org/10.1093/bioinformatics/15.2.174
Salminen MO, Carr JK, Burke DS, McCutchan FE. 1995. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res. Hum. Retroviruses 11(11):1423–1425. https://doi.org/10.1089/aid.1995.11.1423
Sayers K. 2013. On folivory, competition, and intelligence: generalism, overgeneralizations, and models of primate evolution. Primates 54(2):111–124. https://dx.doi.org/10.1007%2Fs10329-012-0335-1
Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, et al. 2012. Insights into hominid evolution from the gorilla genome sequence. Nature 483(7388), 169–175. https://doi.org/10.1038/nature10842
Schoenemann PT. 2006. Evolution of the size and functional areas of the human brain. Annu. Rev. Anthropol. 35(1):379–406. https://doi.org/10.1146/annurev.anthro.35.081705.123210
Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17(12):1246–1247. https://doi.org/10.1093/bioinformatics/17.12.1246
Sikora M, Seguin-Orlando A, Sousa VC, Albrechtsen A, Korneliussen T, Ko A, Rasmussen S, Dupanloup I, Nigst PR, Bosch MD, et al. 2017. Ancient genomes show social and reproductive behavior of early Upper Paleolithic foragers. Science 358(6363):659–662. https://doi.org/10.1126/science.aao1807
Simons EL, Seiffert ER, Ryan TM, Attia Y. 2007. A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae). Proc. Natl. Acad. Sci. USA 104(21):8731–8736. https://doi.org/10.1073/pnas.0703129104
Slatkin M. 2008. Linkage disequilibrium — understanding the evolutionary past and mapping the medical future. Nat. Rev. Genet. 9(6):477–485. https://doi.org/10.1038/nrg2361
Snodgrass JJ, Leonard WR, Robertson ML. 2009. The Energetics of Encephalization in Early Hominids. In: Hublin JJ, Richards MP, editors. The Evolution of Hominin Diets. Integrating Approaches to the Study of Palaeolithic Subsistence. Dordrecht: Springer; p. 15–29.
Somel M, Franz H, Yan Z, Lorenc A, Guo S, Giger T, Kelso J, Nickel B, Dannemann M, Bahn S, et al. 2009. Transcriptional neoteny in the human brain. Proc. Natl. Acad. Sci. USA 106(14):5743–5748. https://doi.org/10.1073/pnas.0900544106
Thornton GK, Woods CG. 2009 Primary microcephaly: do all roads lead to Rome? TIG 25(11):501–510. https://doi.org/10.1016/j.tig.2009.09.011
Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR, Cheung K, Bonné-Tamir B, Santachiara-Benerecetti AS, Moral P, Krings M, et al. 1996. Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science 271(5254):1380–1387. https://doi.org/10.1126/science.271.5254.1380
Walker A, Shipman P. 2005. The Ape in the Tree. An Intellectual and Natural History of Proconsul. Cambridge (MA): Belknap Press of Harvard University Press.
Wang J, Li Y, Su B. 2008. A common SNP of MCPH1 is associated with cranial volume variation in Chinese population. Hum. Mol. Genet. 17(9):1329–1335. https://doi.org/10.1093/hmg/ddn021
Wang YQ, Su B. 2004. Molecular evolution of microcephalin, a gene determining human brain size. Hum. Mol. Genet. 13(11):1131–1137. https://doi.org/10.1093/hmg/ddh127
Ward CV, Flinn M, Begun DR. 2004. Body size and intelligence in hominoid evolution. In: Russon AE, Begun DR, editors. The Evolution of Thought. Evolutionary Origins of Great Ape Intelligence. Cambridge (UK): Cambridge University Press; p. 335–349.
Wilson AC, Bush GL, Case SM, King MC. 1975. Social structuring of mammalian populations and rate of chromosomal evolution. Proc. Natl. Acad. Sci. USA 72(12):5061–5065. https://doi.org/10.1073/pnas.72.12.5061
Wong K. 2006. The morning of the modern mind. Sci. Am. 16(2):74–83. https://doi.org/10.1038/scientificamerican0605-86
Woolfit M. 2009. Effective population size and the rate and pattern of nucleotide substitutions. Biol. Lett. 5:417–420. https://doi.org/10.1098/rsbl.2009.0155
Würsig B. 2002. Intelligence and cognition. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego (CA): Academic Press; p. 628-636.
Xing J, Wang H, Han K, Ray DA, Huang CH, Chemnick LG, Stewart CB, Disotell TR, Ryder OA, Batzer MA. 2005. A mobile element based phylogeny of Old World monkeys. Mol. Phyl. Evolution 37(3):872–880. https://doi.org/10.1016/j.ympev.2005.04.015
Xu S, Chen Y, Cheng Y, Yang D, Zhou X, Xu J, Zhou K, Yang G. 2012. Positive selection at the ASPM gene coincides with brain size enlargements in cetaceans. Proc. Biol. Sci. B 279(1746):4433–4440. https://doi.org/10.1098/rspb.2012.1729
Xu X, Lee J, Stern DF. 2004. Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem. 279(33):34091–34094. https://doi.org/10.1074/jbc.C400139200
Yang Z. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24(8):1586–1591. https://doi.org/10.1093/molbev/msm088
Yang Z, Bielawski JP. 2000. Statistical methods for detecting molecular adaptation. TREE 15(12):496–503. https://doi.org/10.1016/S0169-5347(00)01994-7
Zhang J. 2003. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 165(4):2063–2070. https://doi.org/10.1093/genetics/165.4.2063
Zimin AV, Cornish AS, Maudhoo MD, Gibbs RM, Zhang X, Pandey S, Meehan DT, Wipfler K, Bosinger SE, Johnson ZP, et al. 2014. A new rhesus macaque assembly and annotation for next-generation sequencing analyses. Biol. Direct 9(1):20. https://doi.org/10.1186/1745-6150-9-20
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