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Phylogenomics of African guenons

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Abstract

The karyotypes of 28 specimens belonging to 26 species of Cercopithecinae have been compared with each other and with human karyotype by chromosome banding and, for some of them, by Zoo-FISH (human painting probes) techniques. The study includes the first description of the karyotypes of four species and a synonym of Cercopithecus nictitans. The chromosomal homologies obtained provide us with new data on a large number of rearrangements. This allows us to code chromosomal characters to draw Cercopithecini phylogenetic trees, which are compared to phylogenetic data based on DNA sequences. Our findings show that some of the superspecies proposed by Kingdon (1997 The Kingdon Field Guide to African Mammals, Academic Press.) and Groves (2001 Primates Taxonomy, Smithsonian Institution Press) do not form homogeneous groups and that the genus Cercopithecus is paraphyletic, in agreement with previous molecular analyses. The evolution of Cercopithecini karyotypes is mainly due to non-centromeric chromosome fissions and centromeric shifts or inversions. Non-Robertsonian translocations occurred in C. hamlyni and C. neglectus. The position of chromosomal rearrangements in the phylogenetic tree leads us to propose that the Cercopithecini evolution proceeded by either repeated fission events facilitated by peculiar genomic structures or successive reticulate phases, in which heterozygous populations for few rearranged chromosomes were present, allowing the spreading of chromosomal forms in various combinations, before the speciation process.

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References

  • Amor DJ, Choo HA (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71: 695–714.

    Article  PubMed  Google Scholar 

  • Amor DJ, Bentley K, Ryan J, et al. (2004) Human centromere repositioning ‘in progress’. Proc Natl Acad Sci U S A 101(17): 6542–6547.

    Article  PubMed  CAS  Google Scholar 

  • Anton E, Blanco J, Egozcue J, Vidal F (2005) Sperm studies in heterozygote inversion carriers: a review. Cytogenet Gen Res 111: 297–304.

    Article  CAS  Google Scholar 

  • Arnold ML, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109: 261–276.

    Article  PubMed  Google Scholar 

  • Best RG, Diamond D, Crawford E et al. (1998) Baboon/human homologies examined by spectral karyotyping (SKY): a visual comparison. Cytogenet Cell Genet 82: 83–87.

    Article  PubMed  CAS  Google Scholar 

  • Bigoni F, Stanyon R, Koehler U, Morescalchi AM, Wienberg J (1997) Mapping homology between human and black and white colobine monkey chromosome by fluorescent in situ hybridization. Am J Primatol 42: 289–298.

    Article  PubMed  CAS  Google Scholar 

  • Bremer K (1988) The limits of amino acide sequences data in angiosperm phylogenetics reconstruction. Evolution 42: 795–805.

    Article  CAS  Google Scholar 

  • Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African Cercopithecinae monkeys. Int J Primatol 26(3): 661–684.

    Article  Google Scholar 

  • Disotell TR, Raaum RL (2002) Molecular timescale and gene tree incongruence in the guenons. In: Glenn ME, Cords M, eds. The Guenons: Diversity and Adaptation in African Monkeys. New York: Kluwer Academic/Plenum Publishers, pp. 27–36.

    Google Scholar 

  • Dobigny G, Ducroz J-F, Robinson TJ, Volobouev V (2004) Cytogenetics and Cladistics. Syst Biol 55(3): 470–484.

    Article  Google Scholar 

  • Dutrillaux B, Couturier J (1981) La pratique de l’analyse chromosomique. Paris: Masson, pp. 87.

    Google Scholar 

  • Dutrillaux B, Couturier J (1986) Principes de l’analyse chromosomique appliquée à la phylogénie : l’exemple des Pongidae et des Hominidae. Mammalia 50 numéro spécial: 22–37.

    Google Scholar 

  • Dutrillaux B, Rethore MO, Prieur M, Lejeune J (1973) Analyse de la structure fine des chromosomes du gorille (Gorilla gorilla). Hum Genet 20: 343–354.

    CAS  Google Scholar 

  • Dutrillaux B, Viegas-Pequignot E, Couturier J, Chauvier G (1978) Identity of euchromatic bands from man to Cercopithecidae. Hum Genet 45: 283–296.

    Article  PubMed  CAS  Google Scholar 

  • Dutrillaux B, Couturier J, Chauvier G (1980) Chromosomal evolution of 19 species or sub-species of Cercopithecinae. Ann Genet 23(3): 133–143.

    PubMed  CAS  Google Scholar 

  • Dutrillaux B, Couturier J, Muleris M, Lombard M, Chauvier G (1982) Chromosomal phylogeny of forty-two species or subspecies of Cercopithecoids (Primates, Catarrhini). Ann Genet 25(2): 96–109.

    PubMed  CAS  Google Scholar 

  • Dutrillaux B, Couturier J, Muleris M, Rumpler Y, Viegas-Péquignot E (1986) Relation chromosomiques entre sous-ordre et infra-ordre, et schéma évolutif général des primates. Mammalia 50 numéro spécial: 108–121.

    Google Scholar 

  • Dutrillaux B, Muleris M, Couturier J (1988a) Chromosomal evolution of Cercopithecinae. In: Gautier-Hion A, Bourlière F, Gautier JP, Kingdon J, eds. A Primate Radiation. Evolutionary biology of the African Guenons. New York: Cambridge University Press, pp 150–159.

    Google Scholar 

  • Dutrillaux B, Dutrillaux AM, Lombard M, et al. (1988b) The karyotype of Cercopithecus solatus Harrison 1988, a new species belonging to C. lhoesti, and its phylogenetic relationships with other guenons. J Zool Lond 215: 611–617.

    Google Scholar 

  • Finaz C, Dubois MF, Cochet C, Vignal M, De Grouchy J (1976) Le caryotype du Cercopithèque marquage et nomenclature. Ann Génet 19(3): 213–216.

    PubMed  CAS  Google Scholar 

  • Finelli P, Stanyon R, Plesker R, Ferguson-Smith MA, O’Brien PCM, Wienberg J (1999) Reciprocal chromosome painting shows that the great difference in diploid number between human and African green monkey is mostly due to non-robertsonian fissions. Mamm Genome 10: 713–718.

    Article  PubMed  CAS  Google Scholar 

  • Gautier-Hion A, Bourliere F, Gautier JP, Kingdon J (1988) A Primate Radiation: Evolutionary Biology of the African Guenons. New York: Cambridge University Press.

    Google Scholar 

  • Gerbault-Seureau M, Vielh P, Dutrillaux B (1987) Recurent HSR in the centromeric region of chromosome 8 in breast cancer. Ann Genet 30: 146–151.

    PubMed  CAS  Google Scholar 

  • Gerbault-Seureau M, Bonnet-Garnier A, Richard F, Dutrillaux B (2004) Chromosome painting comparison of Leontopithecus chrysomelas (Callitricine, Platyrrhini) with man and its phylogenetic position. Chromosome Res 12: 691–701.

    Article  Google Scholar 

  • Goidts V, Szamalek JM, deJong PJ et al. (2005) Independent intrachromosomal recombination events underlie the pericentric inversions of chimpanzee and gorilla chromosomes homologous to human chromosome 16. Genome Res 15: 1232–1242.

    Article  PubMed  CAS  Google Scholar 

  • Groves C (2001) Primates Taxonomy. Washington, London: Smithsonian Institution Press, pp. 350.

    Google Scholar 

  • Groves CP (2005) Order Primates. In: Wilson DE, Reeder DA, eds. Mammal Species of the World, A Taxonomic and Geographic Reference, 3rd edn. Baltimore, MD: Johns Hopkins University Press, pp. 152–178.

    Google Scholar 

  • Grubb P (2006) Geospecies and superspecies in the African Primate fauna. Primate Conservation 20: 75–78.

    Article  Google Scholar 

  • Haig D (1999) A brief history of human autosomes. Phil Trans R Soc Lond 354:1447–1470.

    Article  CAS  Google Scholar 

  • Hayes H (1995) Chromosome painting with human chromosome-specific DNA libraries reveals the extent and distribution of conserved segments in bovine chromosomes. Cytogenet Cell Genet 71: 168–174.

    Article  PubMed  CAS  Google Scholar 

  • Jauch A, Weinberg J, Stanyon R et al. (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci U S A 89: 8611–8615.

    Article  PubMed  CAS  Google Scholar 

  • Kingdon J (1997) The Kingdon Field Guide to African Mammals. San Diego: Academic Press.

    Google Scholar 

  • Koblmüller S, Duftner N, Secf CM et al. (2007) Reticulate phylogeny of gastropod-shell-breeding cichlids from lake Tanganyika- the result of repeated introgressive hybridization. BMC Evol Biol 7(7): 1–13.

    Google Scholar 

  • Koehler U, Bigoni F, Wienberg J, Stanyon R (1995) Genomic reorganisation in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30: 287–292.

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Evolutionary history and positional shift of a rice centromere. Genetics 177: 1217–1220.

    Article  PubMed  CAS  Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229–237.

    Article  PubMed  Google Scholar 

  • Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure. J Hum Genet 82(2): 261–282.

    Article  CAS  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH et al. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99(1): 3–10.

    Article  PubMed  CAS  Google Scholar 

  • Montefalcone G, Tempesta S, Rocchi M, Archidiacono N (1999) Centromere repositioning. Genome Res 9: 1184–1188.

    Article  PubMed  CAS  Google Scholar 

  • Morel F, Laudier D, Guerif F, et al. (2007) Meiotic segregation analysis in spermatozoa of pericentric inversion carriers using fluorescence in-situ hybridization. Hum Reprod 22: 136–141.

    Article  PubMed  CAS  Google Scholar 

  • Muleris M, Couturier J, Dutrillaux B (1981) Cytogenetics of Cercopithecus (mona) campbelli campbelli. Comparison with other Cercopithecus species and man. Ann Genet 24(3): 137–140.

    PubMed  CAS  Google Scholar 

  • Muleris M, Gautier JP, Lombard M, Dutrillaux B (1985) étude cytogénétique de Cercopithecus wolfi, Cercopithecus erythrotis et d’un hybride Cercopithecus ascanius x Cercopithecus pogonias grayi. Ann Genet 28(2): 75–80.

    PubMed  CAS  Google Scholar 

  • Müller S, Stanyon R, O’Brien PCM, Ferguson-Smith MA, Plesker R, Weinberg J (1999) Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma 108: 393–400.

    Article  PubMed  Google Scholar 

  • Murnane JP (2006) Telomeres and chromosome instability. DNA Repair 5: 1082–1092.

    Article  PubMed  CAS  Google Scholar 

  • Murphy WJ, Stanyon R, O’Brien SJ (2001) Evolution of mammalian genome organisation inferred from comparative gene mapping. Genome Biol 2(6): 0005.1–0005.8.

    Article  Google Scholar 

  • Nanda I, Schrama D, Feichtinger W (2002) Distribution of telomeric (TTAGGG)n sequences in avian chromosomes. Chromosoma 111: 215–227.

    Article  PubMed  CAS  Google Scholar 

  • Nergadze SG, Rocchi M, Azzalin CM, Mondello C, Giuolotto E (2004) Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Res 14: 1704–1710.

    Article  PubMed  CAS  Google Scholar 

  • Nie W, Rens W, Wang J, Yang F (2001) Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92: 248–253.

    Article  PubMed  CAS  Google Scholar 

  • Nie W, Wang J, O’Brien PCM et al. (2002) The genome phylogeny of domestic cat, red panda and five mustelid species revealed by comparative chromosome painting and G-banding. Chromosome Res 10: 209–222.

    Article  PubMed  CAS  Google Scholar 

  • Popescu P, Hayes H, Dutrillaux B (2000) Techniques of Animal Cytogenetics. INRA Eds, pp 260.

  • Purvis A (1995) A composite estimate of primate phylogeny. Philos Trans R Soc Lond B Biol Sci 348: 405–421.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Dutrillaux B (1998) Origin of the human chromosome 21 and its consequences: a 50-milion-year-old-story. Chromosome Res 6(4): 263–268.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Lombard M, Dutrillaux B (1996) ZOO-FISH suggest a complete homology between human and capuchin monkey (Platyrrhini) euchromatin. Genomics 36: 417–423.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Lombard M, Dutrillaux B (2000) Phylogenetic origin of human chromosomes 7, 16 and 19 and their homologs in placental mammals. Genome Res 10: 644–651.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Lombard M, Dutrillaux B (2003) Reconstruction of the ancestral karyotype of eutherian mammals. Chromosome Res 11: 605–618.

    Article  PubMed  CAS  Google Scholar 

  • Rivera H, Zuffardi O, Maraschio P et al. (1989) Alternate centromere inactivation in a pseudodicentric (15;20) (pter; pter) associated with a progressive neurological disorder. J Med Genet 26: 626–630.

    Article  PubMed  CAS  Google Scholar 

  • Romagno D, Chiarelli B, Guarducci S, Giovannucci Uzielli ML, Sineo L (2000) Chromosome mapping of GBRB3 and PML loci in Macaca and Cercopithecus indicates the mechanism of evolution of human chromosome 15. Chromosome Res 8: 747–749.

    Article  PubMed  CAS  Google Scholar 

  • Robinson TJ, Yang F, Harrison WR (2002) Chromosome painting refines the history of genome evolution in hares and rabbits (order Lagomorpha). Cytogenet Genome Res 96: 223–227.

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Herrera A, Garcia F, Azzalin C et al. (2002) Distribution of intrachromosomal telomeric sequences (ITS) on Macaca fascicularis (Primates) chromosome and their implication for chromosome evolution. Hum Genet 110: 578–586.

    Article  PubMed  CAS  Google Scholar 

  • Rumpler Y, Dutrillaux B (1990) Chromosomal Evolution and Speciation in Primates. In: Guillem E Barbera, ed. Leioa Viscaya, Spain: University of the Basque Country, Springer International, vol. 23.

  • Ruvolo M (1988) Genetic evolution in the African guenons. In: Gautier-Hion A, Bourliere F, Gautier JP, Kingdon J, eds. A Primate Radiation: Evolutionary Biology of the African Guenons. New York: Cambridge University Press, pp. 127–149.

    Google Scholar 

  • Santani A, Raudsepp T, Chowdhary BP (2002) Interstitial telomeric sites and NORs in Hartmann’s zebra (Equus zebra hartmannae) chomosomes. Chromosome Res 10: 527–534.

    Article  PubMed  CAS  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptative radiation Trends Ecol Evol 19: 198–207.

    Article  PubMed  Google Scholar 

  • Shimada MK, Terao K, Shotake T (2002) Mitochondrial sequences diversity within a subspecies of savanna monkeys (Cercopithecus aetiops) is similar to that between subspecies. J Hered 93: 9–18.

    Article  PubMed  CAS  Google Scholar 

  • Sorenson MD, Franzosa EA (2007) TreeRot, version 3. Boston, MA: Boston University.

    Google Scholar 

  • Stanyon R, Bruening R, Stone G, Shearin A, Bigoni F (2005) Reciprocal painting between humans, De Brazza’s and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree. Cytogenet Genome Res 108: 175–182.

    Article  PubMed  CAS  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 304.

    Article  PubMed  CAS  Google Scholar 

  • Swoford DL (2000) PAUP Phylogenetic Analysis Using Parsimony, version 4.β3. Program and documentation. Champaign., IL: Illinois Natural History Survey.

    Google Scholar 

  • Tosi AJ, Morales JC, Melnick J (2000) Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of Macaque evolutionary history. Mol Phylogenet Evol 17(2): 133–144.

    Article  PubMed  CAS  Google Scholar 

  • Tosi AJ, Disotell TR, Morales JC, Melnick DJ (2003) Cercopithecine Y-chromosome data provide a test of competiting morphological evolutionary hypotheses. Mol Phylogenet Evol 27: 510–521.

    Article  PubMed  CAS  Google Scholar 

  • Tosi AJ, Melnick DJ, Disotell TR (2004) Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). J Hum Evol 46: 223–237.

    Article  PubMed  Google Scholar 

  • Tosi AJ, Detwiler KM, Disotell TR (2005) X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini). Mol Phylogenet Evol 36: 58–66.

    Article  PubMed  CAS  Google Scholar 

  • van der Kuyl AC, Kuiken CL, Dekker JT, Goudsmit J (1995) Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences. J Mol Evol 40(2), 173–180.

    Article  PubMed  Google Scholar 

  • van der Kuyl AC, Dekker JT, Goudsmit J (2000) Primate Genus Miopithecus: evidence for the existence of species and subspecies of dwarf guenons based on cellular and endogenous viral sequences. Mol Phylogenet Evol 14(3): 403–413.

    Article  PubMed  CAS  Google Scholar 

  • Ventura M, Archidiacono N, Rocchi M (2001) Centromere emergence in evolution. Genome Res 11: 595–599.

    Article  PubMed  CAS  Google Scholar 

  • Ventura M, Mudge JM, Palumbo V et al. (2003) Neocentromere in 15q24–26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Res 13: 2059–2068.

    Article  PubMed  CAS  Google Scholar 

  • Ventura M, Weigl S, Carbone L et al. (2004) Recurrent sites for new centromere seeding. Genome Res 14: 1696–1703.

    Article  PubMed  CAS  Google Scholar 

  • Ventura M, Antonacci F, Cardone MF et al. (2007) Evolutionary formation of new centromeres in macaque. Science 316: 243–246.

    Article  PubMed  CAS  Google Scholar 

  • Volleth M, Heller KG, Pfeiffer RA, Hameister H (2002) A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families. Chromosome Res 10: 477–497.

    Article  PubMed  CAS  Google Scholar 

  • Warburton PE (2004) Chromosomal dynamics of human neocentromere formation. Chromosome Res 12: 617–626.

    Article  PubMed  CAS  Google Scholar 

  • Wienberg J, Stanyon R, Jauch A, Cremer T (1992) Homologie in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma 101(5–6): 265–270.

    Article  PubMed  CAS  Google Scholar 

  • Wong LH, Choo KHA (2001) Centromere on the move. Genome Res 11: 513–516.

    Article  PubMed  CAS  Google Scholar 

  • Wong LH, Choo KHA (2004) Evolutionary dynamics of transposable elements at the centromere. Tends Genet 20(12): 611–616.

    Article  CAS  Google Scholar 

  • Xing J, Wang H, Zhang Y et al. (2005) A mobile element based phylogeny of Old World Monkeys. Mol Phylogenet Evol 37: 872–880.

    Article  PubMed  CAS  Google Scholar 

  • Xing J, Wang H, Zhang Y et al. (2007) A mobile element-based evolutionary history of guenons (tribe Cercopithecini). BMC Biology 5: 5.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Graphodatsky AS, Li T et al. (2006) Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: further insight into the ancestral karyotype and genome evolution of eutherian mammals. Chromosome Res 14: 283–296.

    Article  PubMed  CAS  Google Scholar 

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Moulin, S., Gerbault-Seureau, M., Dutrillaux, B. et al. Phylogenomics of African guenons. Chromosome Res 16, 783–799 (2008). https://doi.org/10.1007/s10577-008-1226-6

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