Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates)
Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gilbert, C.C.; Bibi, F.; Hill, A.; Beech, M.J. Early guenon from the late Miocene Baynunah Formation, Abu Dhabi, with implications for cercopithecoid biogeography and evolution. Proc. Natl. Acad. Sci. USA 2014, 111, 10119–10124. [Google Scholar] [CrossRef]
- Butynski, T.M. The guenons: An overview of diversity and taxonomy. In The Guenons: Diversity and Adaptation in African Monkeys; Glenn, M.E., Cords, M., Eds.; Kluwer Academic Publishers: New York, NY, USA, 2002; pp. 3–13. [Google Scholar]
- Rusell, A.; Mittermeier, A.B.; Rylands, D.E.W. Handbook of the Mammals of the World; Primates Lynx Edicions: Barcelona, Spain, 2013; Volume 3, ISBN 978-84-96553-89-7. [Google Scholar]
- Lo Bianco, S.; Masters, J.; Sineo, L. The evolution of the cercopithecine: A (post)modern synthesis. Evol. Anthropol. 2017, 26, 336–349. [Google Scholar] [CrossRef] [PubMed]
- Dutrillaux, B.; Muleris, M.; Couturier, J. Chromosomal evolution of Cercopithecinae. In A Primate Radiation: Evolutionary Biology of the African Guenons; Gautier-Hion, A., Bourlière, F., Gautier, J.-P., Eds.; Cambridge University Press: Cambridge, UK, 1988; pp. 150–159. [Google Scholar]
- Dutrillaux, B. Chromosomal evolution in primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum. Genet. 1979, 48, 251–314. [Google Scholar] [CrossRef] [PubMed]
- Stanyon, R.; Bruening, R.; Stone, G.; Shearin, A.; Bigoni, F. Reciprocal painting between humans, De Brazza’s and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree. Cytogenet. Genome Res. 2005, 108, 175–182. [Google Scholar] [CrossRef] [PubMed]
- Tosi, A.J.; Detwiler, K.M.; Disotell, T.R. X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini). Mol. Phylogenetics Evol. 2005, 36, 58–66. [Google Scholar] [CrossRef] [PubMed]
- Tosi, A.J.; Melnick, D.J.; Disotell, T.R. Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). J. Hum. Evol. 2004, 46, 223–237. [Google Scholar] [CrossRef]
- Xing, J.; Wang, H.; Zhang, Y.; Ray, D.A.; Tosi, A.J.; Disotell, T.R.; Batzer, M.A. A mobile element-based evolutionary history of guenons (tribe Cercopithecini). BMC Biol. 2007, 5, 5. [Google Scholar] [CrossRef]
- Cardini, A.; Elton, S. Variation in guenon skulls (I): Species divergence, ecological and genetic differences. J. Hum. Evol. 2008, 54, 615–637. [Google Scholar] [CrossRef]
- Martin, R.D.; McLarnon, A.M. Quantitative comparisons of the skull and teeth in Guenons. In A Primate Radiation: Evolutionary Biology of the African Guenons; Gautier-Hion, A., Ed.; Cambridge University Press: Cambridge, UK, 1988; pp. 160–183. [Google Scholar]
- Dumas, F.; Sineo, L. Chromosomal dynamics in Cercopithecini studied by Williams-Beuren probe mapping. Caryologia 2010, 63, 435–442. [Google Scholar]
- Sineo, L. The Still under Construction Cercopithecinae Phylogeny. J. Primatol. 2012, 1, 2. [Google Scholar] [CrossRef]
- Sineo, L. The banded karyotype of Cercopithecus mitis maesi compared with the karyotypes of C. albogularis samango and C. nictitans stampflii. I. J. Primatol. 1990, 11, 541–552. [Google Scholar]
- Sineo, L.; Lo Bianco, S.; Picone, B. Evidence of a chromosomal polymorphism unique to Cercopithecini. A key factor in the Tribe definition. J. Primatol. 2015, 4. [Google Scholar] [CrossRef]
- Groves, C.P. Primate Taxonomy; Smithsonian Institution Press: Washington, DC, USA, 2001. [Google Scholar]
- Grubb, P.; Butynski, T.M.; Oates, J.F.; Bearder, S.K.; Disotell, T.R.; Groves, C.P.; Struhsaker, T.T. Assessment of the diversity of African primates. Int. J. Primatol. 2003, 24, 1301–1357. [Google Scholar] [CrossRef]
- Takahashi, K.; Terai, Y.; Nishida, M.; Okada, N. Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol. Biol. Evol. 2001, 18, 2057–2066. [Google Scholar] [CrossRef] [PubMed]
- Detwiler, K.M. Hybridization between Red-tailed Monkeys (Cercopithecus ascanius) and Blue Monkeys (C. mitis) in East African Forests. In The Guenons: Diversity and Adaptation in African Monkeys; Glenn, M.E., Cords, M., Eds.; Kluwer Academic Publishers: New York, NY, USA, 2002; p. 79. [Google Scholar]
- Detwiler, K.M. Mitochondrial DNA Analyses of Cercopithecus Monkeys Reveal a Localized Hybrid Origin for C. mitis doggetti in Gombe National Park, Tanzania. Int. J. Primatol. 2019, 40, 28–52. [Google Scholar] [CrossRef]
- De Jong, Y.A.; Butynski, T.M. Three sykes’s monkey Cercopithecus mitis× vervet monkey Chlorocebus pygerythrus hybrids in Kenya. Primate Conserv. 2010, 25, 43–56. [Google Scholar] [CrossRef]
- Furo, I.D.O.; Kretschmer, R.; O’Brien, P.C.; Pereira, J.C.; Ferguson-Smith, M.A.; de Oliveira, E.H.C. Phylogenetic analysis and karyotype evolution in two species of core Gruiformes: Aramides cajaneus and Psophia viridis. Genes 2020, 11, 307. [Google Scholar] [CrossRef]
- Farias, J.C.; Santos, N.; Bezerra, D.P.; Sotero-Caio, C.G. Chromosome Painting in Lonchorhina aurita Sheds Light onto the Controversial Phylogenetic Position of Sword-Nosed Bats (Chiroptera, Phyllostomidae). Cytogenet. Genome Res. 2021, 161, 569–577. [Google Scholar] [CrossRef]
- Knytl, M.; Smolík, O.; Kubíčková, S.; Tlapáková, T.; Evans, B.J.; Krylov, V. Chromosome divergence during evolution of the tetraploid clawed frogs, Xenopus mellotropicalis and Xenopus epitropicalis as revealed by Zoo-FISH. PLoS ONE 2017, 12, e0177087. [Google Scholar] [CrossRef]
- Dumas, F.; Sineo, L.; Ishida, T. Taxonomic identification of Aotus (Platyrrhinae) through cytogenetics, Identificazione tassonomica di Aotus (Platyrrhinae) mediante la citogenetica. J. Biol. Res. Boll. Della Soc. Ital. Biol. Sper. 2015, 88, 65–66. [Google Scholar]
- Dumas, F.; Sineo, L. The evolution of human synteny 4 by mapping sub-chromosomal specific probes in Primates. Caryologia 2014, 67, 281–291. [Google Scholar] [CrossRef]
- Wienberg, J.; Stanyon, R.; Jauch, A.; Cremer, T. Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma 1992, 101, 265–270. [Google Scholar] [CrossRef] [PubMed]
- Wienberg, J. Fluorescence in situ hybridization to chromosomes as a tool to understand human and primate genome evolution. Cytogenet. Genome Res. 2004, 108, 139–160. [Google Scholar] [CrossRef] [PubMed]
- O’Brien, S.J.; Menninger, J.C.; Nash, W.G. Atlas of Mammalian Chromosomes; Wiley-Liss: Hoboken, NJ, USA, 2006. [Google Scholar]
- Moulin, S.; Gerbault-Seureau, M.; Dutrillaux, B.; Richard, F.A. Phylogenomics of African guenons. Chromosome Res. 2008, 16, 783–799. [Google Scholar] [CrossRef] [PubMed]
- Stanyon, R.; Rocchi, M.; Bigoni, F.; Archidiacono, N. Evolutionary molecular cytogenetics of catarrhine primates: Past, present and future. Cytogenet. Genome Res. 2012, 137, 273–284. [Google Scholar] [CrossRef]
- Tolomeo, D.; Capozzi, O.; Chiatante, G.; Sineo, L.; Ishida, T.; Archidiacono, N.; Stanyon, R. Eight million years of maintained heterozygosity in chromosome homologs of cercopithecine monkeys. Chromosoma 2020, 129, 57–67. [Google Scholar] [CrossRef]
- Finelli, P.; Stanyon, R.; Plesker, R.; Ferguson-Smith, M.A.; O’brien, P.; Wienberg, J. 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 1999, 10, 713–718. [Google Scholar] [CrossRef]
- Finelli, P. Analisi citogenetica sulla filogenesi delle catarrhinae tramite ibridazione in situ interspecifiche. In Dissertation; Università Degli Studi di Bari: Bari, Italy, 1996. [Google Scholar]
- Ventura, M.; Antonacci, F.; Cardone, M.F.; Stanyon, R.; D’Addabbo, P.; Cellamare, A.; Sprague, L.J.; Eichler, E.E.; Archidiacono, N.; Rocchi, M. Evolutionary formation of new centromeres in macaque. Science 2007, 316, 243–246. [Google Scholar] [CrossRef]
- Ruiz Herrera, A.; Garcia, F.; Azzalin, C.; Giuliotto, E.; Egozucue JPonsa’, F.M.; Garcia, M. Distribution of intrachromosomal telomeric sequences (ITS) on Macaca fascicularis (Primates) chromosomes and their implication for chromosome evolution. Hum. Genet. 2002, 110, 578–586. [Google Scholar] [CrossRef]
- Dumas, F.; Cuttaia, I.; Sineo, L. Chromosomal distribution of interstitial telomeric sequences in nine neotropical primates (Platyrrhini): Possible implications in evolution and phylogeny. J. Zool. Syst. Evol. Res. 2016, 54, 226–236. [Google Scholar] [CrossRef]
- Mazzoleni, S.; Schillaci, O.; Sineo, L.; Dumas, F. Distribution of interstitial telomeric sequences in primates and the pygmy tree shrew (Scandentia). Cytogenet. Genome Res. 2017, 151, 141–150. [Google Scholar] [CrossRef]
- Ceraulo, S.; Perelman, P.L.; Mazzoleni, S.; Rovatsos, M.; Dumas, F. Repetitive sequence distribution on Saguinus, Leontocebus and Leontopithecus tamarins (Platyrrhine, Primates) by mapping telomeric (TTAGGG) motifs and rDNA loci. Biology 2021, 10, 844. [Google Scholar] [CrossRef]
- Dumas, F.; Perelman, P.L.; Biltueva, L.; Roelke-Parker, M.E. Retrotransposon mapping in spider monkey genomes of the family Atelidae (Platyrrhini, Primates) shows a high level of LINE-1 amplification. J. Biol. Res. Boll. Della Soc. Ital. Biol. Sper. 2022, 95, 10725. [Google Scholar] [CrossRef]
- Dumas, F.; Houck, M.L.; Bigoni, F.; Perelman, P.; Romanenko, S.A.; Stanyon, R. Chromosome painting of the pygmy tree shrew shows that no derived cytogenetic traits link primates and scandentia. Cytogenet. Genome Res. 2012, 136, 175–179. [Google Scholar]
- Ceraulo, S.; Milioto, V.; Dumas, F. Centromeric enrichment of LINE-1 retrotransposon in two species of South American monkeys Alouatta belzebul and Ateles nancymaae (Platyrrhini, Primates). Caryologia 2021, 74, 111–119. [Google Scholar] [CrossRef]
- Ceraulo, S.; Perelman, P.L.; Dumas, F. Massive LINE-1 retrotransposon enrichment in tamarins of the Cebidae family (Platyrrhini, Primates) and its significance for genome evolution. J. Zool. Syst. Evol. Res. 2021, 59, 2553–2561. [Google Scholar] [CrossRef]
- Fernàndez, R.; Barragàn, M.; Bullejos, M.; Marchal, J.; Diaz de la Guardia, R.; Sanchez, A. New C-band protocol by heat denaturation in the presence of formamide. Hereditas 2002, 137, 145–148. [Google Scholar] [CrossRef][Green Version]
- Stanyon, R.; Sineo, L. Citotassonomia e filogenesi del genere Cercopithecus. Antropol. Contemp. 1983, 6, 237–252. [Google Scholar]
- Stanyon, R.; Rocchi, M.; Capozzi, O.; Roberto, R.; Misceo, D.; Ventura, M.; Archidiacono, N. Primate chromosome evolution: Ancestral karyotypes, marker order and neocentromeres. Chromosome Res. 2008, 16, 17–39. [Google Scholar] [CrossRef] [PubMed]
- Graphodatsky, A.S.; Trifonov, V.A.; Stanyon, R. The genome diversity and karyotype evolution of mammals. Mol. Cytogenet. 2011, 4, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Gifalli-Iughetti, C.; Koiffmann, C.P. Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini). Genet. Mol. Biol. 2009, 32, 786–791. [Google Scholar] [CrossRef]
- Capozzi, O.; Archidiacono, N.; Lorusso, N.; Stanyon, R.; Rocchi, M. The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys. Chromosoma 2016, 125, 747–756. [Google Scholar] [CrossRef]
- Romagno, D.; Chiarelli, B.; Sineo, L. Studio Dell’evoluzione dei Cromosomi Dell’uomo Attraverso il Mappaggio di” loci” Specifici Nei Primati Non Umani: Il Caso Del Cromosoma 15. Antropo. 2001; pp. 45–52. Available online: https://dialnet.unirioja.es/servlet/articulo?codigo=4749731 (accessed on 21 February 2023).
- Scardino, R.; Milioto, V.; Proskuryakova, A.A.; Serdyukova, N.A.; Perelman, P.L.; Dumas, F. Evolution of the human chromosome 13 synteny: Evolutionary rearrangements, plasticity, human disease genes and cancer breakpoints. Genes 2020, 11, 383. [Google Scholar] [CrossRef]
- Robinson, T.J.; Ruiz-Herrera, A.; Avise, J.C. Hemiplasy and homoplasy in the karyotypic phylogenies of mammals. Proc. Natl. Acad. Sci. USA 2008, 105, 14477–14481. [Google Scholar] [CrossRef]
Species | EPA (2n = 54) | CAE (2n = 60) | CPE (2n = 66) | CER (2n = 66) | CNE (2n = 62) | CNI (2n = 70) | CWO (2n = 72) |
---|---|---|---|---|---|---|---|
HSA paints | |||||||
1 | 1 | 2 | 3 | 3 | 4 | 3 | 4 |
2 | 2 | 2 | 3 | 3 | 3 | 3 | 3 |
3 | 2 | 2 | 3 | 3 | 3 | 3 | 3 |
4 | 1 | 2 | 1 | 1 | 1 | 2 | 3 |
5 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
6 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
7 | 2 | 2 | 1 | 1 | 1 | 2 | 2 |
8 | 1 | 1 | 2 | 2 | 1 (with 1) | 2 | 1 |
9 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
10 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
11 | 1 | 1 | 2 | 2 | 1 | 2 | 2 |
12 | 1 | 1 | 2 | 2 | 1 | 2 | 2 |
13 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
14 | 1 | 2 | 2 | 2 | 2 | 2 | 2 |
14/15 | + | + | + | + | + | + | + |
15 | 2 | 2 | 1 | 1 | 2 | 1 | 1 |
16 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
17 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
18 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
19 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
20 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
20/21 | + | + | + | + | + | + | + |
21 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
22 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
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Milioto, V.; Sineo, L.; Dumas, F. Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates). Life 2023, 13, 1203. https://doi.org/10.3390/life13051203
Milioto V, Sineo L, Dumas F. Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates). Life. 2023; 13(5):1203. https://doi.org/10.3390/life13051203
Chicago/Turabian StyleMilioto, Vanessa, Luca Sineo, and Francesca Dumas. 2023. "Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates)" Life 13, no. 5: 1203. https://doi.org/10.3390/life13051203
APA StyleMilioto, V., Sineo, L., & Dumas, F. (2023). Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates). Life, 13(5), 1203. https://doi.org/10.3390/life13051203