Comparative Primate Molecular Cytogenetics: Revealing Ancestral Genomes, Marker Order, and Evolutionary New Centromeres

  • Roscoe Stanyon
  • Nicoletta Archidiacono
  • Mariano Rocchi
Part of the Primatology Monographs book series (PrimMono)


In this review, we focus on the cytogenetic level of primate genome organization: chromosomes and karyotypes. Reconstructing the genome of ancestors is an obligatory goal of comparative primate cytogenetics. Cytogenetic comparison between species has a long history, going back to the early decades of the last century. Classical primate cytogeneticists provided basic data on the number of chromosomes, their size, and the relative position of the centromere of many primate species. Chromosome banding showed the high level of conservation among humans, apes, and monkeys, but establishing chromosomal homology between distantly related species or species characterized by rapid chromosomal evolution remained speculative until the advent of molecular cytogenetics. Chromosome painting soon resolved problems of accurately determining chromosomal homology. Painting probes could easily map all the translocation between primate species but did not provide information on intrachromosomal rearrangements. Then, FISH with cloned DNA provided high-resolution cytogenetic comparisons of marker order along chromosomes. Results revealed that centromere shifts (“evolutionary new centromere” ENC) are an important process in modifying primate genomes on a par with translocations and inversions. Comparison between ENC and clinical neocentromeres shows that evolutionary perspectives can provide compelling underlying explicative grounds for contemporary genomic phenomena.


World Monkey Chromosome Painting Diploid Number Ancestral Genome Molecular Cytogenetic 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Bacterial artificial chromosomes


Bacterial artificial chromosome end sequences


Basic local alignment search tool


Contiguous ancestral regions


Chromatin immunoprecipitation


Degenerate oligonucleotide primed-PCR


Evolutionary new centromere


Fluorescence-activated cell sorter


Fluorescent in situ hybridization DNA


P1 artificial chromosomes


Synteny block


Whole chromosome paints


Yeast artificial chromosomes


  1. Amor DJ, Bentley K, Ryan J et al (2004) Human centromere repositioning “in progress”. Proc Natl Acad Sci USA 101:6542–6547PubMedCrossRefGoogle Scholar
  2. Bigoni F, Koehler U, Stanyon R et al (1997a) Fluorescence in situ hybridization establishes homology between human and silvered leaf monkey chromosomes, reveals reciprocal translocations between chromosomes homologous to human Y/5, 1/9, and 6/16, and delineates an X1X2Y1Y2/X1X1X2X2 sex-chromosome system. Am J Phys Anthropol 102:315–327PubMedCrossRefGoogle Scholar
  3. Bigoni F, Stanyon R, Koehler U et al (1997b) Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization. Am J Primatol 42:289–298PubMedCrossRefGoogle Scholar
  4. Capozzi O, Purgato S, Verdun di Cantogno L et al (2008) Evolutionary and clinical neocentromeres: two faces of the same coin? Chromosoma (Berl) 117:339–344CrossRefGoogle Scholar
  5. Capozzi O, Purgato S, D’Addabbo P et al (2009) Evolutionary descent of a human chromosome 6 neocentromere: a jump back to 17 million years ago. Genome Res 19:778–784PubMedCrossRefGoogle Scholar
  6. Carbone L, Nergadze SG, Magnani E et al (2006) Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87:777–782PubMedCrossRefGoogle Scholar
  7. Cardone MF, Alonso A, Pazienza M et al (2006) Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. Genome Biol 7:R91PubMedCrossRefGoogle Scholar
  8. Caspersson T, Zech L, Johansson C et al (1970) Identification of human chromosomes by DNA-binding fluorescent agents. Chromosoma (Berl) 30:215–227CrossRefGoogle Scholar
  9. Chu EHY, Bender MA (1961) Chromosome cytology and evolution in primates. Science 133:1399–1405PubMedCrossRefGoogle Scholar
  10. Darwin C (1859) Origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, LondonGoogle Scholar
  11. Dumas F, Stanyon R, Sineo L et al (2007) Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting. BMC Evol Biol 7(suppl 2):S11PubMedCrossRefGoogle Scholar
  12. Dumas F, Houck ML, Bigoni F et al (2012) Chromosome painting of the pygmy tree shrew shows that no derived cytogenetic traits link Primates and Scandentia. Cytogenet Genome Res (in press)PubMedCrossRefGoogle Scholar
  13. Dutrillaux B (1979) Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum Genet 48:251–314PubMedCrossRefGoogle Scholar
  14. Dutrillaux B, Finaz C, de Grouchy J et al (1972) Comparison of banding patterns of human chromosomes obtained with heating, fluorescence, and proteolytic digestion. Cytogenetics 11:113–116PubMedCrossRefGoogle Scholar
  15. Dutrillaux B, Viegas-Pequignot E, Couturier J (1980) Great homology of chromosome banding of the rabbit (Oryctolagus cuniculus) and primates, including man (author’s translation. Ann Genet 23:22–25PubMedGoogle Scholar
  16. Ferguson-Smith MA, Trifonov V (2007) Mammalian karyotype evolution. Nat Rev Genet 8:950–962PubMedCrossRefGoogle Scholar
  17. Ferguson-Smith MA, Yang F, Rens W et al (2005) The impact of chromosome sorting and painting on the comparative analysis of primate genomes. Cytogenet Genome Res 108:112–121PubMedCrossRefGoogle Scholar
  18. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DCGoogle Scholar
  19. Han Y, Zhang Z, Liu C et al (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci USA 106:14937–14941PubMedCrossRefGoogle Scholar
  20. Huxley TH (1863) Evidence as to man’s place in nature. Williams & Norwood, LondonGoogle Scholar
  21. Jauch A, Wienberg J, Stanyon R et al (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci USA 89:8611–8615PubMedCrossRefGoogle Scholar
  22. Koehler U, Arnold N, Wienberg J et al (1995a) Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization. Am J Phys Anthropol 97:37–47PubMedCrossRefGoogle Scholar
  23. Koehler U, Bigoni F, Wienberg J et al (1995b) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287–292PubMedCrossRefGoogle Scholar
  24. Lomiento M, Jiang Z, D’Addabbo P et al (2008) Evolutionary-new centromeres preferentially emerge within gene deserts. Genome Biol 9:R173PubMedCrossRefGoogle Scholar
  25. Makino S (1952) A contribution to the study of the chromosomes in some Asiatic mammals. Cytologia 16:288–301CrossRefGoogle Scholar
  26. Marshall OJ, Chueh AC, Wong LH et al (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282PubMedCrossRefGoogle Scholar
  27. Misceo D, Capozzi O, Roberto R et al (2008) Tracking the complex flow of chromosome rearrangements from the Hominoidea ancestor to extant Hylobates and Nomascus gibbons by high-resolution synteny mapping. Genome Res 18:1530–1537PubMedCrossRefGoogle Scholar
  28. Montefalcone G, Tempesta S, Rocchi M et al (1999) Centromere repositioning. Genome Res 9:1184–1188PubMedCrossRefGoogle Scholar
  29. Müller S, O’Brien PC, Ferguson-Smith MA et al (1997) Reciprocal chromosome painting between human and prosimians (Eulemur macaco macaco and E. fulvus mayottensis). Cytogenet Cell Genet 78:260–271PubMedCrossRefGoogle Scholar
  30. Müller S, Stanyon R, O’Brien PC et al (1999) Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma (Berl) 108:393–400CrossRefGoogle Scholar
  31. Müller S, Stanyon R, Finelli P et al (2000) Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution. Proc Natl Acad Sci USA 97:206–211PubMedCrossRefGoogle Scholar
  32. Müller S, Hollatz M, Wienberg J (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113:493–501PubMedCrossRefGoogle Scholar
  33. Murphy WJ, Fronicke L, O’Brien SJ et al (2003) The origin of human chromosome 1 and its homologs in placental mammals. Genome Res 13:1880–1888PubMedGoogle Scholar
  34. Neusser M, Stanyon R, Bigoni F et al (2001) Molecular cytotaxonomy of New World monkeys (Platyrrhini): comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet Cell Genet 94:206–215PubMedCrossRefGoogle Scholar
  35. Nie W, Liu R, Chen Y et al (1998) Mapping chromosomal homologies between humans and two langurs (Semnopithecus francoisi and S. phayrei) by chromosome painting. Chromosome Res 6:447–453PubMedCrossRefGoogle Scholar
  36. Nie W, Rens W, Wang J et al (2001) Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92:248–253PubMedCrossRefGoogle Scholar
  37. Nie W, O’Brien PC, Fu B et al (2006) Chromosome painting between human and lorisiform prosimians: evidence for the HSA 7/16 synteny in the primate ancestral karyotype. Am J Phys Anthropol 129:250–259PubMedCrossRefGoogle Scholar
  38. Nie W, Fu B, O’Brien PC et al (2008) Flying lemurs – the ‘flying tree shrews’? Molecular cytogenetic evidence for a Scandentia-Dermoptera sister clade. BMC Biol 6:18PubMedCrossRefGoogle Scholar
  39. O’Brien SJ, Nash WG (1982) Genetic mapping in mammals: chromosome map of domestic cat. Science 216:257–265PubMedCrossRefGoogle Scholar
  40. Roberto R, Capozzi O, Wilson RK et al (2007) Molecular refinement of gibbon genome rearrangement. Genome Res 17:249–257PubMedCrossRefGoogle Scholar
  41. Roberto R, Misceo D, D’Addabbo P et al (2008) Refinement of macaque synteny arrangement with respect to the official rheMac2 macaque sequence assembly. Chromosome Res 16:977–985PubMedCrossRefGoogle Scholar
  42. Rocchi M, Archidiacono N, Stanyon R (2006) Ancestral genomes reconstruction: an integrated, multi-disciplinary approach is needed. Genome Res 16:1441–1444PubMedCrossRefGoogle Scholar
  43. Saffery R, Sumer H, Hassan S et al (2003) Transcription within a functional human centromere. Mol Cell 12:509–516PubMedCrossRefGoogle Scholar
  44. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972PubMedCrossRefGoogle Scholar
  45. She X, Horvath JE, Jiang Z et al (2004) The structure and evolution of centromeric transition regions within the human genome. Nature (Lond) 430:857–864CrossRefGoogle Scholar
  46. Shiwago P (1939) Recherches sur le caryotype du Rhesus macacus. Bull Biol Med Exp (USSR) 9:3–8Google Scholar
  47. Stanyon R, Stone G (2008) Phylogenomic analysis by chromosome sorting and painting. Methods Mol Biol 422:13–29PubMedCrossRefGoogle Scholar
  48. Stanyon R, Wienberg J, Romagno D et al (1992) Molecular and classical cytogenetic analyses demonstrate an apomorphic reciprocal chromosomal translocation in Gorilla gorilla. Am J Phys Anthropol 88:245–250PubMedCrossRefGoogle Scholar
  49. Stanyon R, Bonvicino CR, Svartman M et al (2003) Chromosome painting in Callicebus lugens, the species with the lowest diploid number (2n  =  16) known in primates. Chromosoma (Berl) 112:201–206CrossRefGoogle Scholar
  50. Stanyon R, Bruening R, Stone G et al (2005) Reciprocal painting between humans, De Brazza’s and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree. Cytogenet Genome Res 108:175–182PubMedCrossRefGoogle Scholar
  51. Stanyon R, Dumas F, Stone G et al (2006) Multidirectional chromosome painting reveals a remarkable syntenic homology between the greater galagos and the slow loris. Am J Primatol 68:349–359PubMedCrossRefGoogle Scholar
  52. Stanyon R, Rocchi M, Capozzi O et al (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16:17–39PubMedCrossRefGoogle Scholar
  53. Stock AD, Hsu TC (1973) Evolutionary conservatism in arrangement of genetic material. A comparative analysis of chromosome banding between the rhesus macaque (2n equals 42, 84 arms) and the African green monkey (2n equals 60, 120 arms). Chromosoma (Berl) 43:211–224CrossRefGoogle Scholar
  54. Svartman M, Stone G, Page JE et al (2004) A chromosome painting test of the basal eutherian karyotype. Chromosome Res 12:45–53PubMedCrossRefGoogle Scholar
  55. Trifonov VA, Stanyon R, Nesterenko AI et al (2008) Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Res 16:89–107PubMedCrossRefGoogle Scholar
  56. Ventura M, Mudge JM, Palumbo V et al (2003) Neocentromeres in 15q24-26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Res 13:2059–2068PubMedCrossRefGoogle Scholar
  57. Ventura M, Weigl S, Carbone L et al (2004) Recurrent sites for new centromere seeding. Genome Res 14:1696–1703PubMedCrossRefGoogle Scholar
  58. Ventura M, Antonacci F, Cardone MF et al (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246PubMedCrossRefGoogle Scholar
  59. Wienberg J, Stanyon R (1997) Comparative painting of mammalian chromosomes. Curr Opin Genet Dev 7:784–791PubMedCrossRefGoogle Scholar
  60. Wienberg J, Stanyon R, Jauch A et al (1992) Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma (Berl) 101:265–270CrossRefGoogle Scholar
  61. Yeager CH, Painter TS, Yerkes RM (1940) The chromosomes of the chimpanzee. Science 91:74–75PubMedCrossRefGoogle Scholar
  62. Yu D, Yang F, Liu R (1997) A comparative chromosome map between human and Hylobates hoolock built by chromosome painting. Yi Chuan Xue Bao 24:417–423PubMedGoogle Scholar
  63. Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2012

Authors and Affiliations

  • Roscoe Stanyon
    • 1
  • Nicoletta Archidiacono
    • 2
  • Mariano Rocchi
    • 2
  1. 1.Laboratory of Anthropology, Department of Evolutionary BiologyUniversity of FlorenceFlorenceItaly
  2. 2.Department of Genetics and MicrobiologyUniversity of BariBariItaly

Personalised recommendations