Skip to main content
Log in

Interspecific Chromosome Painting Provides Clues to the Ancestral Karyotype of the New World Monkey Genus Aotus

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The Neotropical monkey genus Aotus (owl or night monkeys) are among the most karyological diverse primates of the world. Their diploid numbers range from 2n = 46 to 58, but even owl monkeys with the same diploid number may have radically different karyotypes. This karyotypic variability has provided precious information for taxonomists and has a potential for aiding phylogenetic analysis of these primates. However, up to now only three out of 11 species have been analyzed with molecular cytogenetic methods. Here, we report on a fourth species, A. infulatus. Females have a diploid number of 2n = 50 while males, due to a Y/autosome translocation, have 49 chromosomes. We provide a complete map of chromosome homology between humans and A. infulatus. Comparisons with previous reports allowed us to propose a putative ancestral karyotype of the genus (2n = 52) and to deduce the rearrangements that were involved in the origin of each species chromosome complement. Integration of chromosome painting and banding analysis suggests at least three chromosomes have evolutionary new centromeres that appeared during the divergence of these four owl monkey species.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Araújo NP, Loss AC, Cordeiro-Junior DA, da Silva KR, Leite YLR, Svartman M (2014) New karyotypes of Atlantic tree rats, genus Phyllomys (Rodentia: Echimyidae). Genome 57:1–8

    Article  CAS  PubMed  Google Scholar 

  • Capozzi O, Archidiacono N, Lorusso N, Stanyon R, Rocchi M (2016) The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys. Chromosoma 125:747–756

  • de Oliveira EHC, Neusser M, Müller S (2012) Chromosome evolution in New World monkeys (Platyrrhini). Cytogenet Genome Res 137:259–272

  • Dumas F, Bigoni F, Stone G, Sineo L, Stanyon R (2005) Mapping genomic rearrangements in titi monkeys by chromosome flow sorting and multidirectional in-situ hybridization. Chromosome Res 13:85–96

    Article  CAS  PubMed  Google Scholar 

  • Hershkovitz P (1949) Mammals of northern Colombia. Preliminary report no. 4: Monkeys (primates) with taxonomic revisions of some forms. Proc US Natl Mus 98:323–427

    Article  Google Scholar 

  • Hershkovitz P (1983) Two new species of night monkeys, genus Aotus (Cebidae, Platyrrhini): a preliminary report on Aotus taxonomy. Am J Primatol 4:209–243

  • Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: A 1-step method. Experientia 36:1014–1015

    Article  CAS  PubMed  Google Scholar 

  • Kiesling NMJ, Yi SV, Xu K, Sperone FG, Wildman DE (2014) The tempo and mode of New World monkey evolution and biogeography in the context of phylogenomic analysis. Mol Phylogenet Evol 82:386–399

  • Ma NSF (1981) Chromosome evolution in the owl monkey, Aotus. Am J Phys Anthropol 54:293–303

    Article  Google Scholar 

  • Ma NSF, Aquino R, Collins WE (1985) Two new karyotypes in the Peruvian owl monkey (Aotus trivirgatus). Am J Primatol 9:333–341

    Article  Google Scholar 

  • Ma NSF, Elliott MW, Morgan L, Miller A, Jones TC (1976) Translocation of Y chromosome to an autosome in the Bolivian owl monkey, Aotus. Am J Phys Anthropol 45:191–202

  • Menezes AN, Bonvicino CR, Seuánez HN (2010) Identification, classification and evolution of owl monkeys (Aotus, Illiger 1811). BMC Evol Biol 10:248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mudry MD, Nieves M, Bolzán AD (2007) Chromosomal localization of the telomeric (TTAGGG)n sequence in eight species of New World primates (Neotropical primates, Platyrrhini). Cytogenet Genome Res 119:221–224

  • Osterholz M, Walter L, Roos C (2009) Retropositional events consolidate the branching order among New World monkey genera. Mol Phylogenet Evol 50:507–513

  • Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MAM, Kessin 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieczarka JC, Barros RMS, Faria FM Jr, Nagamachi CY (1993) Aotus from the southwestern Amazon region is geographically and chromosomally intermediate between A. azarae boliviensis and A. infulatus. Primates 34:197–204

    Article  Google Scholar 

  • Pieczarka JC, Nagamachi CY (1988) Cytogenetic studies of Aotus from eastern Amazonia: Y/autosome rearrangement. Am J Primatol 14:255–263

    Article  Google Scholar 

  • Prakhongcheep O, Chaiprasertsri N, Terada S, Hirai Y, Srikulnath K, Hirai H, Kogo A (2013) Heterochromatin blocks constituting the entire short arms of acrocentric chromosomes of Azara’s owl monkey: formation processes inferred from chromosomal locations. DNA Res 20:461–470

  • Ruiz-Herrera A, García F, Aguilera M, Garcia M, Fontanals MP (2005) Comparative chromosome painting in Aotus reveals a highly derived evolution. Am J Primatol 65:73–85

    Article  PubMed  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972

    Article  CAS  PubMed  Google Scholar 

  • Springer MS, Meredith RW, Gatesy J, Emerling CA, Park J, Rabosky DL, Stadler T, Steiner C, Ryder OA, Janecka JE, Fisher CA, Murphy WJ (2012) Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS One 7(11): e49521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanyon R, Bigoni F, Slaby T, Muller S, Stone G, Bonvicino CR, Neusser M, Seuánez HN (2004) Multi-directional chromosome painting maps homologies between species belonging to three genera of New World monkeys and humans. Chromosoma 113:305–315

  • Stanyon R, Bonvicino CR, Svartman M, Seuánez HN (2003) Chromosome painting in Callicebus lugens, the species with the lowest diploid number (2n=16) known in primates. Chromosoma 112:201–206

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Galleni L (1991) A rapid fibroblast culture technique for high resolution karyotypes. Boll Zool 58:81–83

    Article  Google Scholar 

  • Stanyon R, Garofalo F, Steinberg ER, Capozzi O, Di Marco S, Nieves M, Archidiacono N, Mudry MD (2011) Chromosome painting in two genera of South American monkeys: species identification, conservation, and management. Cytogenetic Genome Res 134:40–50

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:305–306

    Article  Google Scholar 

  • Torres OM, Enciso S, Ruiz F, Silva E, Yunis I (1998) Chromosome diversity of the genus Aotus from Colombia. Am J Primatol 44:255–275

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Process 4072622013-0) to MS and RS and a PRIN (Programmi di Ricerca Scientifica di Rilevante Interesse Nazionale: 2012TZF8HL_003) to RS. NPA was the recipient of a doctoral fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marta Svartman.

Ethics declarations

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

This article does not contain any studies with human participants performed by any of the authors.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Araújo, N.P., Stanyon, R., do Socorro Pereira, V. et al. Interspecific Chromosome Painting Provides Clues to the Ancestral Karyotype of the New World Monkey Genus Aotus. J Mammal Evol 26, 283–290 (2019). https://doi.org/10.1007/s10914-017-9403-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-017-9403-z

Keywords

Navigation