Skip to main content
Log in

Chromosome painting in Callicebus lugens, the species with the lowest diploid number (2n=16) known in primates

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Cytogenetic studies have shown that New World primates are karyologically diverse and highly derived. The genus Callicebus is the best example of this karyological diversity, with diploid numbers ranging from 2n=50 to 2n=16. We report on Callicebus lugens, which has the lowest diploid number (2n=16) yet found in the primate order and represents a striking example of extreme karyotypic shuffling. To better understand the genomic rearrangements that have resulted in this extremely low diploid number, we mapped chromosome homologies between C. lugens and humans by in situ hybridization. The total number of hybridization signals was 42, excluding the Y chromosome, with a total of 34 syntenic associations not found in humans. This species has one of the most derived karyotypes among the Platyrrhini. Fusion has been the predominant mode of karyological evolution, although fissions and inversions have also transformed the C. lugens karyotype. Remarkably in such a highly rearranged karyotype, the synteny of 11 human chromosomes (4, 5, 9, 12, 13, 14, 17, 18, 20, 21, and X) was maintained intact, even if most of these human-homologous gene clusters were translocated. Other human syntenies, such as homologues to human chromosomes 10 and 16, were highly fragmented. Comparisons of the C. lugens-human homology map with those of other New World primates have not yet helped establish a phylogenic arrangement between congeneric species or link Callicebus with any other genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Barros RM, Nagamachi CY, Pieczarka JC, Rodrigues LR, Neusser M, de Oliveira EH, Wienberg J, Muniz JA, Rissino JD, Muller S (2003) Chromosomal studies in Callicebus donacophilus pallescens, with classic and molecular cytogenetic approaches: multicolour FISH using human and Saguinus oedipus painting probes. Chromosome Res 11:327–334

    Article  CAS  PubMed  Google Scholar 

  • Bonvicino CR, Penna-Firme V, Nascimento FF, Lemos B, Stanyon R, Seuanez HN (2003) The lowest diploid number (2n=16) yet found in any primate: Callicebus lugens (Humboldt 1811). Folia Primatol (Basel) 74:141–149

    Google Scholar 

  • Chu EHY, Bender MA (1962) Cytogenetics and evolution of primates. Ann NY Acad Sci 102:253–266

    CAS  PubMed  Google Scholar 

  • Consigliere S, Stanyon R, Koehler U, Agoramoorthy G, Wienberg J (1996) Chromosome painting defines genomic rearrangements between red howler monkey subspecies. Chromosome Res 4:264–270

    CAS  PubMed  Google Scholar 

  • Consigliere S, Stanyon R, Koehler U, Arnold N, Wienberg J (1998) In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini, Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes. Am J Primatol 46:119–133

    CAS  PubMed  Google Scholar 

  • Dutrillaux B, Couturier J, Viegas-Pequignot E (1986) Evolution chromosomique des Platyrrhiniens. Mammalia 50:56–81

    Google Scholar 

  • Ford SM (1986) Systematics of the New World monkeys. In: Swindler DR, Erwin J (eds) Systematics, evolution and anatomy. Liss, New York, pp 73–135

  • Garcia F, Ruiz-Herrera A, Egozcue J, Ponsa M, Garcia M (2002) Chromosomal homologies between Cebus and Ateles (primates) based on ZOO-FISH and G-banding comparisons. Am J Primatol 57:177–188

    Article  CAS  PubMed  Google Scholar 

  • Hershkovitz P (1963) A systematic and zoogeographic account of the monkeys of the genus Callicebus (Cebidae) of the Amazonas and Orinoco River basins. Mammalia 27:1–80

    Google Scholar 

  • Hershkovitz P (1988) Origin, speciation, dispersal of South American titi monkeys, genus Callicebus (family Cebidae, Platyrrhini. Proc Acad Sci Phil 140:240–272

    Google Scholar 

  • Hershkovitz P (1990) Titis, New World monkeys of the genus Callicebus (Cebidae, Platyrrhini) a preliminary taxonomic review. Field Zool 55:1–109

    Google Scholar 

  • Kay RF (1990) The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea). J Hum Evol 4:448–456

    Google Scholar 

  • Koiffmann CP, Saldanha PH (1981) The karyotype of Cacajao melanocephalus (Platyrrhini, Primates). Folia Primatol (Basel) 36:150–155

    Google Scholar 

  • Morescalchi MA, Schempp W, Consigliere S, Bigoni F, Wienberg J, Stanyon R (1997) Mapping chromosomal homology between humans and the black-handed spider monkey by fluorescence in situ hybridization. Chromosome Res 5:527–536

    CAS  PubMed  Google Scholar 

  • Muller S, Stanyon R, O’Brien PC, Ferguson-Smith MA, Plesker R, Wienberg 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Neusser M, Stanyon R, Bigoni F, Wienberg J, Muller S (2001) Molecular cytotaxonomy of New World monkeys (Platyrrhini)—comparative analysis of five species by multicolor chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet Cell Genet 94:206–215

    Article  CAS  PubMed  Google Scholar 

  • O’Brien SJ, Stanyon R (1999) Phylogenomics. Ancestral primate viewed. Nature 402:365–366

    Article  CAS  PubMed  Google Scholar 

  • Oliveira EH de, Neusser M, Figueiredo WB, Nagamachi C, Pieczarka JC, Sbalqueiro IJ, Wienberg J, Muller S (2002) The phylogeny of howler monkeys (Alouatta, Platyrrhini): reconstruction by multicolor cross-species chromosome painting. Chromosome Res 10:669–683

    Article  PubMed  Google Scholar 

  • Rodrigues LR, Barros RM, Pissinatti A, Pieczarka JC, Nagamachi CY (2001) Cytogenetic study of Callicebus hoffmannsii (Cebidae, Primates) and comparison with C. m. moloch. Cytobios 105:137–145

    CAS  PubMed  Google Scholar 

  • Roosmalen MGM van, van Roosmalen T, Mittermeier RA (2002) A taxonomic review of the titi monkeys, genus Callicebus (Thomas 1903), with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neotrop Primates 10 [Suppl]:1–52

  • Rosenberger AL, Coimbra-Filho AF (1984) Morphology, taxonomic status and affinities of the lion tamarins, Leontopithecus (Callitrichinae, Cebidae). Folia Primatol 42:149–179

    Google Scholar 

  • Rosenberger AL, Setoguchi T, Shigehara N (1990) The fossil record of callitrichine primates. J Hum Evol 19:209–223

    Google Scholar 

  • Schneider H, Canavez FC, Sampaio I, Moreira MA, Tagliaro CH, Seuanez HN (2001) Can molecular data place each neotropical monkey in its own branch? Chromosoma 109:515–523

    CAS  PubMed  Google Scholar 

  • Seuanez HN, Lima CR, Lemos B, Bonvicino CR, Moreira MA, Canavez FC (2001) Gene assignment in Ateles paniscus chamek (Platyrrhini, Primates). Allocation of 18 markers of human syntenic groups 1, 2, 7, 14, 15, 17 and 22. Chromosome Res 9:631–639

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Consigliere S, Muller S, Morescalchi A, Neusser M, Wienberg J (2000) Fluorescence in situ hybridization (FISH) maps chromosomal homologies between the dusky titi and squirrel monkey. Am J Primatol 50:95–107

    CAS  PubMed  Google Scholar 

  • Telenius H, Pelmear AH, Tunnacliffe A, Carter NP, Behmel A, Ferguson-Smith MA, Nordenskjold M, Pfragner R, Ponder BA (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4:257–263

    CAS  PubMed  Google Scholar 

Download references

Acknowledgement

Work was supported by Instituto Nacional de Câncer, Fundação Ary Frauzino and PRONEX (Brazil).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Stanyon.

Additional information

Communicated by S. Henikoff

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stanyon, R., Bonvicino, C.R., Svartman, M. et al. Chromosome painting in Callicebus lugens, the species with the lowest diploid number (2n=16) known in primates. Chromosoma 112, 201–206 (2003). https://doi.org/10.1007/s00412-003-0261-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-003-0261-5

Keywords

Navigation