SpringerLink
Log in

The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys

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

Abstract

Fluorescence in situ hybridization (FISH), especially chromosome painting, has been extensively exploited in the phylogenetic reconstruction of primate evolution. Although chromosome painting is a key method to map translocations, it is not effective in detecting chromosome inversions, which may be up to four times more frequent than other chromosomal rearrangements. BAC-FISH instead can economically delineate marker order and reveal intrachromosomal rearrangements. However, up to now, BAC-FISH was rarely used to study the chromosomes of New World monkeys partly due to technical difficulties. In this paper, we used BAC-FISH to disentangle the complex evolutionary history of the ancestral 14/15 association in NWMs, beginning from the squirrel monkey (Saimiri boliviensis). To improve the hybridization efficiency of BAC-FISH in NWMs, we “translated” the human BACs into Callithrix jacchus (CJA) BACs, which yielded much higher hybridization efficiencies on other NWM species than human BACs. Our results disclosed 14 synteny blocks in squirrel monkeys, 7 more than with chromosome painting. We then applied a subset of CJA BACs on six other NWM species. The comparison of the hybridization pattern of these species contained phylogenetic information to discriminate evolutionary relationships. Notably Aotus was found to share an inversion with Callithrix, thus definitely assigning the genus Aotus to Cebidae. The present study can be seen as a paradigmatic approach to investigate the phylogenetics of NWMs by molecular cytogenetics.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Amaral PJS, Finotelo LFM, De Oliveira EHC, Pissinatti A, Nagamachi CY, Pieczarka JC (2008) Phylogenetic studies of the genus Cebus (Cebidae-Primates) using chromosome painting and G-banding. BMC Evol Biol 8:169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee HJ, Ho SY, Barnes I, Groves C (2009) Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol Biol 9:259

    Article  PubMed  PubMed Central  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Davis BW, Raudsepp T, Pearks Wilkerson AJ, Agarwala R, Schaffer AA, Houck M, Chowdhary BP, Murphy WJ (2009) A high-resolution cat radiation hybrid and integrated FISH map** resource for phylogenomic studies across Felidae. Genomics 93:299–304

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira EH, Neusser M, Muller S (2012) Chromosome evolution in new world monkeys (Platyrrhini). Cytogenet Genome Res 137:259–272

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dumas F, Stanyon R, Sineo L, Stone G, Bigoni F (2007) Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting. BMC Evol Biol 7(Suppl 2):S11

    Article  PubMed  PubMed Central  Google Scholar 

  • Faraut T (2008) Addressing chromosome evolution in the whole-genome sequence era. Chromosome Res 16:5–16

    Article  CAS  PubMed  Google Scholar 

  • Garcia F, Nogues C, Ponsa M, Ruiz-Herrera A, Egozcue J, Garcia Caldes M (2000) Chromosomal homologies between humans and Cebus apella (Primates) revealed by ZOO-FISH. Mamm Genome 11:399–401

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Giannuzzi G, Pazienza M, Huddleston J, Antonacci F, Malig M, Vives L, Eichler EE, Ventura M (2013) Hominoid fission of chromosome 14/15 and the role of segmental duplications. Genome Res 23:1763–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gifalli-Iughetti C, Koiffmann CP (2009) Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini). Genet Mol Biol 32:786–791

    Article  PubMed  PubMed Central  Google Scholar 

  • Graphodatsky A, Ferguson-Smith MA, Stanyon R (2012) A short introduction to cytogenetic studies in mammals with reference to the present volume. Cytogenet Genome Res 137:83–96

    Article  CAS  PubMed  Google Scholar 

  • Groves CP (2005) Order Primates. Johns Hopkins University Press

  • Jameson Kiesling NM, Yi SV, Xu K, Gianluca Sperone F, Wildman DE (2015) The tempo and mode of New World monkey evolution and biogeography in the context of phylogenomic analysis. Mol Phylogenet Evol 82:386–399

    Article  PubMed  Google Scholar 

  • Jauch A, Wienberg J, Stanyon R, Arnold N, Tofanelli S, Ishida T, Cremer T (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci U S A 89:8611–8615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morescalchi MA, Schempp W, Consigliere S, Bigoni F, Wienberg J, Stanyon R (1997) Map** chromosomal homology between humans and the black-handed spider. Chromosome Res 5:527–536

    Article  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  CAS  PubMed  Google Scholar 

  • Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G, Auvil L, Beever JE, Chowdhary BP, Galibert F, Gatzke L, Hitte C, Meyers SN, Milan D, Ostrander EA, Pape G, Parker HG, Raudsepp T, Rogatcheva MB, Schook LB, Skow LC, Welge M, Womack JE, O'Brien SJ, Pevzner PA, Lewin HA (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617

    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 multi-color 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 

  • Nie W, O'Brien PC, Fu B, Wang J, Su W, Ferguson-Smith MA, Robinson TJ, Yang F (2005) Chromosome painting between human and lorisiform prosimians: evidence for the HSA 7/16 synteny in the primate ancestral karyotype. Am J Phys Anthropol 129:250–259

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MAM, Kessing 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:e1001342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez SI, Klaczko J, dos Reis SF (2012) Species tree estimation for a deep phylogenetic divergence in the New World monkeys (Primates: Platyrrhini). Mol Phylogenet Evol 65:621–630

    Article  PubMed  Google Scholar 

  • Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F, Mazzagatti A, Perini G, Della Valle G, Nergadze SG, Sullivan KF, Raimondi E, Rocchi M, Giulotto E (2015) Centromere sliding on a mammalian chromosome. Chromosoma 124:277–287

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ray DA, **ng J, Hedges DJ, Hall MA, Laborde ME, Anders BA, White BR, Stoilova N, Fowlkes JD, Landry KE, Chemnick LG, Ryder OA, Batzer MA (2005) Alu insertion loci and platyrrhine primate phylogeny. Mol Phylogenet Evol 35:117–126

    Article  CAS  PubMed  Google Scholar 

  • Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Herrera A, Farre M, Robinson TJ (2012) Molecular cytogenetic and genomic insights into chromosomal evolution. Heredity (Edinb) 108:28–36

    Article  CAS  Google Scholar 

  • Rylands AB, Mittermeier RA (2014) Primate taxonomy: species and conservation. Evol Anthropol 23:8–10

    Article  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:e49521

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Rocchi M, Capozzi O, Roberto R, Misceo D, Ventura M, Cardone M, Bigoni F, Archidiacono N (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16:17–39

    Article  CAS  PubMed  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. Cytogenet Genome Res 134:40–50

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Rocchi M, Bigoni F, Archidiacono N (2012) Evolutionary molecular cytogenetics of catarrhine primates: past, present and future. Cytogenet Genome Res 137:273–284

    Article  CAS  PubMed  Google Scholar 

  • Ventura M, Mudge JM, Palumbo V, Burn S, Blennow E, Pierluigi M, Giorda R, Zuffardi O, Archidiacono N, Jackson MS, Rocchi M (2003) Neocentromeres in 15q24-26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Res 13:2059–2068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Worley KC, Warren WC, Rogers J, Locke D, Muzny DM et al (2014) The common marmoset genome provides insight into primate biology and evolution. Nat Genet 46:850–857

    Article  Google Scholar 

Download references

Acknowledgments

“PRIN 2012” funding from Ministero dell'Istruzione dell'Università e della Ricerca is acknowledged.

Author information

Authors and Affiliations

  1. Department of Biology, University of Bari, Bari, Italy

    Oronzo Capozzi, Nicoletta Archidiacono, Nicola Lorusso & Mariano Rocchi

  2. Department of Biology, University of Florence, Florence, Italy

    Roscoe Stanyon

Authors
  1. Oronzo Capozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicoletta Archidiacono
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicola Lorusso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roscoe Stanyon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mariano Rocchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Roscoe Stanyon or Mariano Rocchi.

Ethics declarations

International, national, and institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. 1

Co-hybridization experiment on Saimiri boliviensis preparation of painting probes specific for human chromosome 14 (green) and 15 (red). The FISH signal are on SBO chromosomes 2 and 7. The arrow indicate the 15B fragment of human chromosome 15 on SBO7. (JPG 303 kb)

Supplemental Table 1

List of all genomic clones used in FISH experiments to characterize the synteny organization of the 14/15 association in 7 NWM species, specified in the first row, columns E-K (SBO = Saimiri boliviensis; CCP = Cebus capucinus; CAP = Cebus apella; ALE = Aotus lemurinus griseimembra; CJA = Callithrix jacchus; LLA = Lagothrix lagothrica; CMO = Callicebus moloch). The genomic clones are ordered according to their position (hg19) on the human chromosomes 15 (top) or 14 (bottom) (column D). Clones of the marmoset library CH259 are positioned also on the marmoset genome assembly CalJac3, as reported in UCSC database. For each clone is also reported its cytogenetic position (p or q arm, columns E-K). Yellow lines indicate a synteny breakage in that species, that can be species specific or shared with other species. Synteny breaks in Saimiri are numbered in column L. Synteny blocks generated by these breakpoints are numbered in column A in alphabetical order. (PDF 54 kb)

Supplemental Table 2

Synteny blocks organization on the q arm of Saimiri boliviensis chromosome 2. Clones of the marmoset library CH259 are positioned also on the marmoset genome assembly CalJac3, as reported in UCSC database. For each clone is also reported its cytogenetic position (p or q arm, column E). Yellow lines indicate a synteny breakage. Clones of the marmoset library CH259 are positioned also on the marmoset genome assembly CalJac3, as reported in UCSC database. (PDF 48 kb)

Supplemental Table 3-5

Each Table lists of genomic clones mapped on chromosome 8 of Aotus lemurinus (Supplemental Table 3), chromosome 6 of Cebus capucinus (Supplemental Table 4),and chromosome 6 of Cebus apella (Supplemental Table 5). Yellow lines indicate a synteny breakage. Clones of the marmoset library CH259 are positioned also on the marmoset genome assembly CalJac3, as reported in UCSC database (PDF 40 kb)

(PDF 39 kb)

(PDF 38 kb)

Supplemental Table 6

(PDF 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Capozzi, O., Archidiacono, N., Lorusso, N. et al. The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys. Chromosoma 125, 747–756 (2016). https://doi.org/10.1007/s00412-015-0565-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-015-0565-2

Keywords

Search

Navigation