The evolution of brain size among the Homininae and selection at ASPM and MCPH1 genes

Authors

  • Sandra Leyva-Hernández Escuela Nacional de Antropología e Historia, Ciudad de México, México; Procuraduría General de Justicia del Estado de Guanajuato, Guanajuato, México
  • Ricardo Fong-Zazueta Escuela Nacional de Antropología e Historia, Ciudad de México, México; Laboratorio de Antropología Genética. Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de México, Ciudad de México, México
  • Luis Medrano-González Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, México https://orcid.org/0000-0002-8217-5095
  • Ana Julia Aguirre-Samudio Laboratorio de Antropología Genética. Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de México, Ciudad de México, México https://orcid.org/0000-0002-6674-5641

DOI:

https://doi.org/10.37819/biosis.002.02.0104

Keywords:

Brain size, Homo, Microcephaly-associated genes, Molecular evolution, Natural selection

Abstract

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.

References

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

Graphical abstract

Downloads

Additional Files

Published

2021-06-22

How to Cite

Leyva-Hernández, S. ., Fong-Zazueta, R. ., Medrano-González, L. ., & Aguirre-Samudio, A. J. . (2021). The evolution of brain size among the Homininae and selection at ASPM and MCPH1 genes . Biosis: Biological Systems, 2(2), 293-310. https://doi.org/10.37819/biosis.002.02.0104