Abstract
Unbiased readings of fossils are well known to contradict some of the popular molecular groupings among primates, particularly with regard to great apes and tarsiers. The molecular methodologies today are however flawed as they are based on a mistaken theoretical interpretation of the genetic equidistance phenomenon that originally started the field. An improved molecular method the ‘slow clock’ was here developed based on the Maximum Genetic Diversity hypothesis, a more complete account of the unified changes in genotypes and phenotypes. The method makes use of only slow evolving sequences and requires no uncertain assumptions or mathematical corrections and hence is able to give definitive results. The findings indicate that humans are genetically more distant to orangutans than African apes are and separated from the pongid clade ∼17.6 million years ago. Also, tarsiers are genetically closer to lorises than simian primates are. Finally, the fossil times for the radiation of mammals at the K/T boundary and for the Eutheria-Metatheria split in the Early Cretaceous were independently confirmed from molecular dating calibrated using the fossil split times of gorilla-orangutan, mouse-rat, and opossum-kangaroo. Therefore, the re-established primate phylogeny indicates a remarkable unity between molecules and fossils.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Simons E L. The phyletic position of Ramapithecus. Postilla, 1961, 57: 1–9
Simons E L, Pilbeam D R. Preliminary revision of the Dryopithecinae (Pongidae, Anthropoidea). Folia Primatol (Basel), 1965, 3: 81–152
Pilbeam D. The earliest hominids. Nature, 1968, 219: 1335–1338
Schwartz J H. The evolutionary relationships of man and orang-utans. Nature, 1984, 308: 501–505
Lewin R. Human Evolution. 5th ed. Malden: Blackwell Publishing Ltd., 2005
Schwartz J H. The Red Ape, Orangutans and Human Origins. Cambridge: Westview Press, 2005
Goodman M. Immunochemistry of the primates and primate evolution. Ann N Y Acad Sci, 1962, 102: 219–234
Sarich V M, Wilson A C. Immunological time scale for hominid evolution. Science, 1967, 158: 1200–1203
Wilson A C, Sarich V M. A molecular time scale for human evolution. Proc Natl Acad Sci USA, 1969, 63: 1088–1093
Margoliash E. Primary structure and evolution of cytochrome c. Proc Natl Acad Sci USA, 1963, 50: 672v679
Huang S. The overlap feature of the genetic equidistance result, a fundamental biological phenomenon overlooked for nearly half of a century. Biol Theory, 2010, 5: 40–52
Kimura M. Evolutionary rate at the molecular level. Nature, 1968, 217: 624–626
Huang S. Histone methylation and the initiation of cancer. In: Tollefsbol T, ed. Cancer Epigenetics., New York: CRC Press, 2008
Huang S. Inverse relationship between genetic diversity and epigenetic complexity. Preprint available at Nature Precedings 2009. http://dx.doi.org/10.1038/npre.2009.1751.2
Copley R R, Schultz J, Ponting C P, et al. Protein families in multicellular organisms. Curr Opin Struct Biol, 1999, 9: 408–415
Huang S. The genetic equidistance result of molecular evolution is independent of mutation rates. J Comp Sci Syst Biol, 2008, 1: 92–102
Brunet M, Guy F, Pilbeam D, et al. A new hominid from the Upper Miocene of Chad, Central Africa. Nature, 2002, 418: 145–151
Suwa G, Kono R T, Katoh S, et al. A new species of great ape from the late Miocene epoch in Ethiopia. Nature, 2007, 448: 921–924
Shoshani J, Groves C P, Simons E L, et al. Primate phylogeny: morphological vs. molecular results. Mol Phylogenet Evol, 1996, 5: 102–154
Schwartz J H. How close are the similarities between Tarsius and other primates? In: Wright P C, Simons E L, Gursky S, eds. Tarsiers: Past, Present and Future. Piscataway: Rutgers University Press, 2003
Bininda-Emonds O R, Cardillo M, Jones K E, et al. The delayed rise of present-day mammals. Nature, 2007, 446: 507–512
Wible J R, Rougier G W, Novacek M J, et al. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary. Nature, 2007, 447: 1003–1006
Flynn J J, Parrish J M, Rakotosamimanana B, et al. A new Middle Jurassic mammals from Madagascar. Nature, 1999, 401: 57–60
Kumar S, Hedges S B. A molecular timescale for vertebrate evolution. Nature, 1998, 392: 917–920
Luo Z X, Ji Q, Wible J R, et al. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science, 2003, 302: 1934–1940
Benton M J, Donoghue P C. Paleontological evidence to date the tree of life. Mol Biol Evol, 2007, 24: 26–53
Chatterjee H J, Ho S Y W, Barnes I, et al. Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol Biol, 2009, 9: 259
Bajpai S, Kay R F, Williams B A, et al. The oldest Asian record of Anthropoidea. Proc Natl Acad Sci USA, 2008, 105: 11093–11098
Sige B, Jaeger J J, Sudre J, et al. Altiatlasius koulchii n. gen. et sp., primate omomyidé du Paléocène supérieur du Maroc, et les origines des euprimates. Palaeontographica Abt A, 1990, 214: 31–56
Beard C. The Hunt for the Dawn Monkey. Berkeley: University of California Press, 2004
Kay R F, Ross C, Williams B A. Anthropoid origins. Science, 1997, 275: 797–804
Luo Z X, Yuan C X, Meng Q J, et al. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature, 2011, 476: 442–445
Wildman D E, Uddin M, Liu G, et al. Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc Natl Acad Sci USA, 2003, 100: 7181–7188
Elango N, Thomas J W, Yi S V. Variable molecular clocks in hominoids. Proc Natl Acad Sci USA, 2006, 103: 1370–1375
Collard M, Wood B. How reliable are human phylogenetic hypotheses? Proc Natl Acad Sci USA, 2000, 97: 5003–5006
Grehan J R. Mona Lisa smile: the morphological enigma of human and great ape evolution. Anat Rec B New Anat, 2006, 289: 139–157
Lebatard A E, Bourles D L, Duringer P, et al. Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: Mio-Pliocene hominids from Chad. Proc Natl Acad Sci USA, 2008, 105: 3226–3231
White T D, Asfaw B, Beyene Y, et al. Ardipithecus ramidus and the paleobiology of early hominids. Science, 2009, 326: 75–86
Cela-Conde C J, Ayala F J. Human Evolution: Trails from the Past. Oxford: Oxford University Press, 2007
Stringer C, Andrews P. The Completer World of Human Evolution. New York: Thames and Hudson, 2005
Schwartz J H. The origins of human bipedalism. Science, 2007: 1065
Thorpe S K, Holder R L, Crompton R H. Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science, 2007, 316: 1328–1331
McBrearty S, Jablonski N G. First fossil chimpanzee. Nature, 2005, 437: 105–108
Smith T M, Martin L B, Leakey M G. Enamel thickness, microstructure and development in Afropithecus turkanensis. J Hum Evol, 2003, 44: 283–306
Enard W, Khaitovich P, Klose J, et al. Intra- and interspecific variation in primate gene expression patterns. Science, 2002, 296: 340–343
Uddin M, Wildman D E, Liu G, et al. Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc Natl Acad Sci USA, 2004, 101: 2957–2962
Karaman M W, Houck M L, Chemnick L G, et al. Comparative analysis of gene-expression patterns in human and African great ape cultured fibroblasts. Genome Res, 2003, 13: 1619–1630
Yunis J J, Prakash O. The origin of man: a chromosomal pictorial legacy. Science, 1982, 215: 1525–1530
Marques-Bonet T, Kidd J M, Ventura M, et al. A burst of segmental duplications in the genome of the African great ape ancestor. Nature, 2009, 457: 877–881
Bull J J, Badgett M R, Wichman H A, et al. Exceptional convergent evolution in a virus. Genetics, 1997, 147: 1497–1507
Bollback J P, Huelsenbeck J P. Parallel genetic evolution within and between bacteriophage species of varying degrees of divergence. Genetics, 2009, 181: 225–234
Castoe T A, de Koning A P, Kim H M, et al. Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci USA, 2009, 106: 8986–8991
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Biographical Sketch
Dr. Huang Shi was a professor at the State Key Laboratory of Medical Genetics at Central South University in Changsha, China. He grew up in the army compound of the Chinese Academy of Military Medicine in Beijing where his father was a professor. His childhood interest was however not medicine but sports and later fine arts. An unsuccessful effort in the entrance examination of the Chinese Central Academy of Fine Arts in 1978 changed his interest to science. He entered Fudan University in 1979 and graduated in 1983 with a bachelor’s degree in genetics. He was a CUSBEA fellow of Class III (1984) and obtained his Ph.D. in biochemistry at the University of California at Davis in 1988. After finishing a postdoctoral training at the University of California at San Diego, he was appointed in 1992 assistant professor at the Sanford-Burnham Institute and promoted to associate professor in 1998. He was appointed professor at Central South University in 2009. The early training in art helped shape his taste in aesthetics and interest in science only as a creative endeavor. His laboratory discovered the RIZ or PRDM family of histone methyltransferases and proposed an epigenetic pathway of carcinogenesis by diet rich in meat and low in vegetables. Since 2003, he initiated study of the relationship between genetics and epigenetics and its role in the evolution of biological complexity. He proposed the maximum genetic diversity hypothesis and has been using it to rewrite evolution and population genetics as well as to solve genetic puzzles of complex traits/diseases about which the existing paradigm is clueless. He was one of the 1993 class of Pew Scholars in the Biomedical Sciences.
Electronic supplementary material
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Huang, S. Primate phylogeny: molecular evidence for a pongid clade excluding humans and a prosimian clade containing tarsiers. Sci. China Life Sci. 55, 709–725 (2012). https://doi.org/10.1007/s11427-012-4350-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-012-4350-7