We explored the topology of 18S and 28S rDNA units by fluorescence in situ hybridization (FISH) in the karyotypes of thirteen species representatives from major groups of Primates and Tupaia minor (Günther, 1876) (Scandentia), in order to expand our knowledge of Primate genome reshuffling and to identify the possible dispersion mechanisms of rDNA sequences. We documented that rDNA probe signals were identified on one to six pairs of chromosomes, both acrocentric and metacentric ones. In addition, we examined the potential homology of chromosomes bearing rDNA genes across different species and in a wide phylogenetic perspective, based on the DAPI-inverted pattern and their synteny to human. Our analysis revealed an extensive variability in the topology of the rDNA signals across studied species. In some cases, closely related species show signals on homologous chromosomes, thus representing synapomorphies, while in other cases, signal was detected on distinct chromosomes, leading to species specific patterns. These results led us to support the hypothesis that different mechanisms are responsible for the distribution of the ribosomal DNA cluster in Primates.

Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche Università degli Studi di Palermo via Archirafi

Faculty of Science Department of Ecology Viničná 7 Charles University Pragha 2 Czech Republic

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Baicharoen S, Hirai Y, Srikulnath K, Kongprom U, Hirai H. (2016) Hypervariability of Nucleolus Organizer Regions in Bengal Slow Lorises, Nycticebus bengalensis (Primates, Lorisidae). Cytogenetic and Genome Research 149(4): 267–273. https://doi.org/10.1159/000449145 PubMed DOI

Bedard MT, Ma NSF, Jones TC. (1978) Chromosome Banding Patterns and Nucleolar Organizing Regions in Three Species of Callithricidae. Journal of Medical Primatology 7: 82–97. https://doi.org/10.1159/000459791 PubMed DOI

Bigoni F, Stanyon R, Koehler U, Morescalchi AM, Wienberg J. (1997) Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization. American Journal of Primatology 42(4): 289–298. https://doi.org/10.1002/(SICI)1098-2345(1997)42:4<289::AID-AJP4>3.0.CO;2-T PubMed DOI

Britton-Davidian J, Cazaux B, Catalan J. (2012) Chromosomal dynamics of nucleolar organizer regions (NORs) in the house mouse: micro-evolutionary insights. Heredity (Edinb) 108(1): 68–74. https://doi.org/10.1038/hdy.2011.105 PubMed DOI PMC

Bulatova N, Pavlova S. (2016) A possible cytogenetic analogy to genomic «speciation islands» as revealed by chromosome study of a natural hybrid vole. Tsitologiya 58(5): 412–415. PubMed

Cardone MF, Ventura M, Tempesta S, Rocchi M, Archidiacono N. (2002) Analysis of chromosome conservation in Lemur catta studied by chromosome paints and BAC/PAC probes. Chromosoma 111(5): 348–56. https://doi.org/10.1007/s00412-002-0215-3 PubMed DOI

Cazaux B, Catalan J, Veyrunes F, Douzery EJ, Britton-Davidian J. (2011) Are ribosomal DNA clusters rearrangement hotspots?: a case study in the genus Mus (Rodentia, Muridae). BMC Evolutionary Biology 11(1): 124. https://doi.org/10.1186/1471-2148-11-124 PubMed DOI PMC

Cioffi MB, Martins C, Bertollo LA. (2010) Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus Implications for genome change and karyoevolution in fish. BMC Evolutionary Biology 10(1): 271. https://doi.org/10.1186/1471-2148-10-271 PubMed DOI PMC

Da Silva Calixto M, de Andrade IS, Cabral-de-Mello DC, Santos N, Martins C, Loreto V, de Souza MJ. (2014) Patterns of rDNA and telomeric sequences diversification: Contribution to repetitive DNA organization in Phyllostomidae bats. Genetica 142(1): 49–58. https://doi.org/10.1007/s10709-013-9753-2 PubMed DOI

De Oliveira EHC, Neusser M, Figueiredo WB, Nagamachi C, Pieczarka JC, Sbalqueiro IJ, Pieczarka JC, Sbalqueiro IJ, Wienberg J, Müller S. (2002) The phylogeny of howler monkeys (Alouatta, Platyrrhini): Reconstruction by multicolor cross-species chromosome painting. Chromosome Research 10(8): 669–683. https://doi.org/10.1023/A:1021520529952 PubMed DOI

De Oliveira EHC, Neusser M, Pieczarka JC, Nagamachi C, Sbalqueiro IJ, Müller S. (2005) Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus. Cytogenetic and Genome Research 108(1–3): 183–190. https://doi.org/10.1159/000080814 PubMed DOI

Degrandi TM, Pita S, Panzera Y, De Oliveira EHC, Marques JRF, Figueiró MR, Marques LC, Vinadé Lucia, Gunski RJ, del Valle Garnero A. (2014) Karyotypic evolution of ribosomal sites in buffalo subspecies and their crossbreed. Genetics and Molecular Biology 37(2): 375–380. https://doi.org/10.1590/S1415-47572014000300009 PubMed DOI PMC

Dumas F, Houck ML, Bigoni F, Perelman P, Romanenko SA, Stanyon R. (2012) Chromosome painting of the pygmy tree shrew shows that no derived cytogenetic traits link primates and scandentia. Cytogenetic and Genome Research 136(3): 175–179. https://doi.org/10.1159/000336976 PubMed DOI

Dumas F, Cuttaia H, Sineo L. (2016) Chromosomal distribution of interstitial telomeric sequences in nine neotropical primates (Platyrrhini): possible implications in evolution and phylogeny. Journal of Zoological Systematics and Evolutionary Research (3): 226–236. https://doi.org/10.1111/jzs.12131 DOI

Averbeck KT, Eickbush TH. (2005) Monitoring the mode and tempo of concerted evolution in the Drosophila melanogaster rDNA locus. Genetics 171: 1837–1846. https://doi.org/10.1534/genetics.105.047670 PubMed DOI PMC

Eickbush TH, Eickbush DG. (2007) Finely orchestrated movements: Evolution of the ribosomal RNA genes. Genetics 175(2): 477–485. https://doi.org/10.1534/genetics.107.071399 PubMed DOI PMC

Endow SA. (1982) Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics 100: 375–385. PubMed PMC

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. Mammalian Genome 10(7): 713–718. https://doi.org/10.1007/s003359901077 PubMed DOI

Gornung E, Bezerra AMR, Castiglia R. (2011) Comparative chromosome mapping of the rRNA genes and telomeric repeats in three Italian pine voles of the Microtus savii s.l. complex (Rodentia, Cricetidae). Comparative Cytogenetics 5(3): 247–257. https://doi.org/10.3897/compcytogen.v5i3.1429 PubMed DOI PMC

Guillén AKZ, Hirai Y, Tanoue T, Hirai H. (2004) Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Research 12: 225–237. https://doi.org/10.1023/B:CHRO.0000021911.43225.eb PubMed DOI

Henderson AS, Atwood KC, Warburton D. (1976) Chromosomal Distribution of rDNA in Pan paniscus, Gorilla gorilla beríngeí, and Symphalangus syndactylus: Comparison to Related Primates. Chromosoma 59: 147–155. https://doi.org/10.1007/BF00328483 PubMed DOI

Henderson AS, Warburton D, Megraw-Ripley S, Atwood KC. (1977) The chromosomal location of rDNA in selected lower primates. Cytogenetics and Cell Genetics 19: 281–302. https://doi.org/10.1159/000130821 PubMed DOI

Henderson AS, Warburton D, Megraw-Ripley S, Atwood KC. (1979) The chromosomal location of rDNA in the Sumatran orangutan, Pongo pygmaeus albei. Cytogenetics and Cell Genetics 23: 213–216. https://doi.org/10.1159/000131328 PubMed DOI

Henderson AS, Warburton D, Atwood KC. (1974) Localization of rDNA in the Chimpanzee (Pan troglodytes) chromosome complement. Chromosome 46: 135–441. https://doi.org/10.1007/BF00331631 PubMed DOI

Henderson AS, Warburton D, Atwood KC. (1972) Location of ribosomal DNA in the human chromosome complement. Proceedings of the National Academy of Sciences 69: 3394–3398. https://doi.org/10.1073/pnas.69.11.3394 PubMed DOI PMC

Hirai H, Yamamoto MT, Taylor RW, Imai H. (1996) Genomic dispersion of 28S rDNA during karyotypic evolution on the ant genus Myrmecia (Formicidae). Chromosoma 105: 190–196. https://doi.org/10.1007/BF02509500 PubMed DOI

Hirai H, Hasegawa Y, Kawamoto Y, Tokita E. (1998) Tandem duplication of nucleolus organizer region (NOR) in the Japanese macaque Macaca fuscata fuscata. Chromosome Research 6: 191–197. https://doi.org/10.1023/A:1009207600920 PubMed DOI

Hirai H, Taguchi T, Godwin AK. (1999) Genomic differentiation of 18S ribosomal DNA and β-satellite DNA in the hominoid and its evolutionary aspects. Chromosome Research 7: 531–540. https://doi.org/10.1023/A:1009237412155 PubMed DOI

Hirai H, Hirai Y, Domae H, Kirihara Y. (2007) A most distant intergeneric hybrid offspring (Larcon) of lesser apes, Nomascus leucogenys and Hylobates lar. Human Genetics 122: 477–483. https://doi.org/10.1007/s00439-007-0425-0 PubMed DOI

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. Proceedings of the National Academy of Sciences 89(18): 8611–8615. https://doi.org/10.1073/pnas.89.18.8611 PubMed DOI PMC

Lin J, Chen G, Gu L, Shen Y, Zheng M, Zheng W, Jiang C. (2014) Phylogenetic affinity of tree shrews to Glires is attributed to fast evolution rate. Molecular Phylogenetics and Evolution 71(1): 193–200. https://doi.org/10.1016/j.ympev.2013.12.001 PubMed DOI

Maddison WP, Maddison DR. (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org

Masters JC, Stanyon R, Romagno D. (1987) Standardized karyotypes for the greater Galagos, Galago crassicaudatus E. Geoffroy, 1812 and G. garnettii (Ogilby, 1838) (Primates: Prosimii). Genetica 75(2): 123–129. https://doi.org/10.1007/BF00055256 PubMed DOI

Mazzoleni S, Schillaci O, Sineo L, Dumas F. (2017) Distribution of Interstitial Telomeric Sequences in Primates and the Pygmy Tree Shrew (Scandentia). Cytogenetic and Genome Research 151: 141–150. https://doi.org/10.1159/000467634 PubMed DOI

Müller S, Hollatz M, Wienberg J. (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Human Genetics 113(6): 493–501. https://doi.org/10.1007/s00439-003-0997-2 PubMed DOI

Nagamachi CY, Pieczarka JC, de Sousa Barros RM. (1992) karyotypic comparison cebuella, Callithrix jacchus and C. emilia (Callitrichidae, Primates) and its taxomic implication. Genetica 85: 249–257. https://doi.org/10.1007/BF00132277 PubMed DOI

Neusser M, Stanyon R, Bigoni F, Wienberg J, Müller 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. Cytogenetics and Cell Genetics 94(3–4): 206–215. https://doi.org/10.1159/000048818 PubMed DOI

Nguyen TT, Aniskin VM, Gerbault-Seureau M, Planton H, Renard JP, Nguyen BX, Volobouev VT. (2008) Phylogenetic position of the saola (Pseudoryx nghetinhensis) inferred from cytogenetic analysis of eleven species of Bovidae. Cytogenetic and Genome Research 122(1): 41–54. https://doi.org/10.1159/000151315 PubMed DOI

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, Slattery JP. (2011) A molecular phylogeny of living primates. PLoS Genetics 7: 1–17. https://doi.org/10.1371/journal.pgen.1001342 PubMed DOI PMC

Robicheau BM, Susko E, Harrigan AM, Snyder M. (2017) Ribosomal RNA Genes Contribute to the Formation of Pseudogenes and Junk DNA in the Human Genome. Genome biology and evolution 9(2): 380–397. https://doi.org/10.1093/gbe/evw307 PubMed DOI PMC

Rovatsos M, Johnson Pokorná M, Altmanová M, Kratochvíl L. (2015a) Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): differentiation of sex and neo-sex chromosomes. Scientific Reports 5: 13196. https://doi.org/10.1038/srep13196 PubMed DOI PMC

Rovatsos M, Johnson Pokorná M, Kratochvíl L. (2015b) Differentiation of Sex Chromosomes and Karyotype Characterisation in the Dragonsnake Xenodermus javanicus (Squamata: Xenodermatidae). Cytogenetic and Genome Research 147(1): 48–54. https://doi.org/10.1159/000441646 PubMed DOI

Rovatsos M, Johnson Pokorná M, Altmanová M, Kratochvíl L. (2016) Mixed-Up Sex Chromosomes: Identification of Sex Chromosomes in the X1X1X2X2/X1X2Y System of the Legless Lizards of the Genus Lialis (Squamata: Gekkota: Pygopodidae). Cytogenetic and Genome Research 149(4): 282–289. https://doi.org/10.1159/000450734 PubMed DOI

Schempp W, Zeitler S, Rietschel W. (1998) Chromosomal localization of rDNA in the gorilla. Cytogenetics and Cell Genetics 80: 185–187. https://doi.org/10.1159/000014977 PubMed DOI

Sember A, Bohlen J, Slechtová V, Altmanová M, Symonová R, Ráb P. (2015) Karyotype differentiation in 19 species of river loach fishes Nemacheilidae, Teleostei): extensive variability associated with rDNA and heterochromatin distribution and its phylogenetic and ecological interpretation. BMC Evolutionary Biology 15(1): 251. https://doi.org/10.1186/s12862-015-0532-9 PubMed DOI PMC

Sineo L, Dumas F, Vitturi R, Picone B, Privitera O, Stanyon R. (2007) Williams-Beuren mapping in Callithrix argentata, Callicebus cupreus and Alouatta caraya indicates different patterns of chromosomal rearrangements in neotropical primates. Journal of Zoological Systematics and Evolutionary Research 45(4): 366–371. https://doi.org/10.1111/j.1439-0469.2007.00408.x DOI

Small MF, Stanyon R, Smith DG, Sineo L. (1985) High resolution chromosomes of rhesus macaques (Macaca mulatta). American Journal of Primatology 9: 63–67. https://doi.org/10.1002/ajp.1350090107 PubMed DOI

Srikulnath K, Matsubara K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Nishida C. (2009) Karyological characterization of the butterfly lizard (leiolepis reevesii rubritaeniata, agamidae, squamata) by molecular cytogenetic approach. Cytogenetic and Genome Research 125(3): 213–223. https://doi.org/10.1159/000230005 PubMed DOI

Srikulnath K, Uno Y, Matsubara K, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y. (2011) Chromosomal localization of the 18S-28S and 5S rRNA genes and (TTAGGG) n sequences of butterfly lizards (Leiolepis belliana belliana and Leiolepis boehmei, Agamidae, Squamata). Genetics and Molecular Biology 34(4): 583–586. https://doi.org/10.1590/S1415-47572011005000042 PubMed DOI PMC

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. Cytogenetic and Genome Research 108(1–3): 175–182. https://doi.org/10.1159/000080813 PubMed DOI

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. American Journal of Primatology 50(2): 95–107. https://doi.org/10.1002/(SICI)1098-2345(200002)50:2<95::AID-AJP1>3.0.CO;2-8 PubMed DOI

Stanyon R, Koehler U, Consigliere S. (2002) Chromosome painting reveals that galagos have highly derived karyotypes. American Journal of Physical Anthropology 117: 319–326. https://doi.org/10.1002/ajpa.10047 PubMed DOI

Stults DM, Killen MW, Pierce HH, Pierce AJ. (2008) Genomic architecture and inheritance of human ribosomal RNA gene clusters. Genome Research 18: 13–18. https://doi.org/10.1101/gr.6858507 PubMed DOI PMC

Tantravahi R, Miller DA, Dev VG, Miller OJ. (1976) Detection of nucleolus organizer regions in chromosomes of human, chimpanzee, gorilla, orangutan and gibbon. Chromosoma 56: 15–27. https://doi.org/10.1007/BF00293725 PubMed DOI

Tanomtong A, Khunsook S, Supanuam P, Kaewsri S. (2009) A novel polymorphism of nuclear organizer regions (NORs) and complex inversion chromosome 8 of white-hended gibbons (Hylobates lar, Linnaeus, 1771) in Thailand. Cytologia 74(4): 379–384. https://doi.org/10.1508/cytologia.74.379 DOI

Warburton D, Henderson AS, Atwood KC. (1975) Localization of rDNA and giemsa-banded chromosome complement of white-handed gibbon, Hylobates lar. Chromosoma 51(1): 35–40. https://doi.org/10.1007/BF00285805 PubMed DOI

Zhou X, Sun F, Xu S, Yang G, Li M. (2015) The position of tree shrews in the mammalian tree: Comparing multi-gene analyses with phylogenomic results leaves monophyly of Euarchonta doubtful. Integrative Zoology 10(2): 186–198. https://doi.org/10.1111/1749-4877.12116 PubMed DOI

A Fish of Multiple Faces, Which Show Us Enigmatic and Incredible Phenomena in Nature: Biology and Cytogenetics of the Genus Carassius

Repetitive Sequence Distribution on Saguinus, Leontocebus and Leontopithecus Tamarins (Platyrrhine, Primates) by Mapping Telomeric (TTAGGG) Motifs and rDNA Loci

Cytogenetic Evidence for Sex Chromosomes and Karyotype Evolution in Anguimorphan Lizards

Universal fluorescence in situ hybridization (FISH) protocol for mapping repetitive DNAs in insects and other arthropods

Molecular Cytogenetic Characterization of the Sicilian Endemic Pond Turtle Emys trinacris and the Yellow-Bellied Slider Trachemys scripta scripta (Testudines, Emydidae)