Abstract
Saguinus is the largest and most complex genus of the subfamily Callitrichinae, with 23 species distributed from the south of Central America to the north of South America with Saguinus midas having the largest geographical distribution while Saguinus bicolor has a very restricted one, affected by the population expansion in the state of Amazonas. Considering the phylogenetic proximity of the two species along with evidence on the existence of hybrids between them, as well as cytogenetic studies on Saguinus describing a conserved karyotypic macrostructure, we carried out a physical mapping of DNA repeated sequences in the mitotic chromosome of both species, since these sequences are less susceptible to evolutionary pressure and possibly perform an important function in speciation. Both species presented 2n = 46 chromosomes; in S. midas, chromosome Y is the smallest. Multiple ribosomal sites occur in both species, but chromosome pairs three and four may be regarded as markers that differ the species when subjected to G banding and distribution of retroelement LINE 1, suggesting that it may be cytogenetic marker in which it can contribute to identification of first generation hybrids in contact zone. Saguinus bicolor also presented differences in the LINE 1 distribution pattern for sexual chromosome X in individuals from different urban fragments, probably due to geographical isolation. In this context, cytogenetic analyses reveal a differential genomic organization pattern between species S. midas and S. bicolor, in addition to indicating that individuals from different urban fragments have been accumulating differences because of the isolation between them.
Similar content being viewed by others
References
Ayres JM, Mittermeier RA, Constable ID (1982) Brazilian Tamarins on the way to extinction? Orix 16:329–333
Bedard MT, Ma NSF, Jones TC (1978) Chromosome banding patterns and nucleolar organizing regions in three species of Callithrichidae (Saguinus oedipus, Saguinus fuscicollis and Callithrix jacchus). J Med Primatol 7:82–97
Benirschke K, Brownhill LE (1962) Further observations on marrow chimerism in marmosets. Cytogenetics 1:245–257
Benirschke K, Kumamoto AT, Esra GN, Woods F (1982) The chromosomes of the emperor tamarin, Saguinus imperator Goeldi,1907. Zool Gart Jena 52:168–174.
Birchler JA, Bhadra MP, Bhadra U (2000) Making noise about silence: repression of repeated genes in animals. Curr Opin Genet Dev 10:211–216
Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff J-N (2008) Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16(1):203–215
Boissinot S, Entezam A, Furano AV (2001) Selection against deleterious LINE-1-containing loci in the human lineage. Mol Biol Evol 18:926–935
Boissinot S, Roos C, Furano AV (2004) Different rates of LINE-1 (L1) retrotransposon amplification and evolution in New World monkeys. J Mol Evol 58:122–130
Boisvert FM, van Koningsbruggen S, Navascués J (2007) The multifuncional nucleolus. Nature Rev 8:574–585
Boyle AL, Ballard SG, Ward DC (1990) Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc Natl Acad Sci 87:7757–7761
Canavez FC, Moreira MAM, Simon F, Parham P, Seuánez HN (1999) Phylogenetic relationship of the Callitrichinae (Platyrrhini, Primates) beta2-microglobulin DNA sequence. Am J Primatol 48:225–236
Céspedes SP, Mena DMM, Ortiz JBL (2012) Karyotype of tití grey (Saguinus leucopus) through r-replicate bands. Rev Fac Nac Agron 65:2
Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KHA, Wong LH (2009) LINE retrotransposon RNA Is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 51:e1000354
Dantas SMMM, Barros RMS (1997) Cytogenetic study of the genus Saguinus (Callithrichidae, Primates), Brazilian. J Genet 20:4
de Oliveira JB (2014) Filogeografia e Demografia Histórica de Saguinus bicolor. Master Thesis. Instituto Nacional de Pesquisa da Amazônia
Dutrillaux B, Couturier J, Viegas-Péquignot E (1986) Evolution chromosomique des Platyrrhiniens. Mammalia 50:56–58
Ferguson-Smith MA (2015) History and evolution of cytogenetics. Mol Cytogenet 20:8–19
Gold JR, Li YC, Shipley NS, Powers PK (1990) Improved methods for working with fish chromosomes with a review of metaphase chromosome banding. J Fish Biol 37:563–575
Grewal SIS, Jia S (2007) Heterochromatin revised. Nat Rev Genet 8:35–46
Gross MC, Schneider CH, Valente GT, Porto JIR, Martins C, Feldberg E (2010) Variability of 18 S rDNA locus among Symphysodon fishes: chromosomal rearrangements. J Fish Biol 76:1117–1127
Han JS, Boeke JD (2005) LINE-1 retrotransposons: modulators of quantity and quality of mammalian gene expression? Bioessays 27:775–784
Henikoff S, Malik HS (2002) Centromeres: selfish drivers. Nature 417:227
Hershkovitz P (1977) Living New World Monkey (Platyrrhini). Universal of the Chicago—USA. v.1
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
IJdo JW, Baldini A, Ward DC, Reeders ST, Wells RA (1991) Origin of human chromosome 2: an ancestral telomere-telomere fusion. P Natl A Sci 88(20):9051–9055
Jacobs-Cropp S, Larson A, Cheverud JM (1999) Historical biogeography of tamarins, genus Saguinus: the molecular phylogenetic evidence. Am J Phys Anthropol 108:65–89
Jurka J (2004) Evolutionary impact of human Alu repetitive elements. Curr Opin Genet Dev 14:603–608
Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632
Korenberg JR, Rykowski MC (1988) Human genome organization: Alu, lines, and the molecular structure of metaphase chromosome bands. Cell 53:391–400
Kvikstad EM, Makova KD (2010) The (r)evolution of SINE versus LINE distributions in primate genomes: sex chromosomes are important. Genoma Res 20(5):600–613
Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220
Meireles CMM, Sampaio MIC, Schneider H, Ferrari SF, Coimbra-filho AF, Pissinatti A, Schneider MPC (1997) A comparative study of eleven protein systems in tamarins, genus Saguinus (Platyrrhini, Callitrichinae). Braz J Genet 20(1):13
Moorhead PS, Nowell PC, Mellmam WJ, Battips DM, Hungerford DA (1960) Chromosome preparations of leukocytes cultured from human peripheral blood. Exp Cell Res 20:613–616
Nagamachi CY, Pieczarka JC (1988) Chromosome studies of Saguinus midas niger (Callithrichidae, Primates) from Tucurui, Para, Brazil: comparison with the karyotype of Callithrix jacchus. Am J Primatol 14:277–284
Nagamachi CY, Pieczarka JC, Barros RMS (1990) Cytogenetic study of Saguinus midas midas (Callithrichidae, Primates) from Jari, Brazilian Amazonia. Comparison with the karyotype of Saguinus midas niger. Rev Bras Genet 13:89–96
Nagamachi CY, Pieczarka JC, Schwarz M, Barros RMS, Mattevi EMS (1997) Chromosomal similarities and differences between tamarins, Leontopithecus and Saguinus (Platyrrhini, Primates). Am J Primatol 43:265–276
Nagamachi CY, Pieczarka JC, Muniz JA, Barros RMS, Mattevi MS (1999) Proposed chromosomal phylogeny for the south American primates of the Callitrichidae family (Platyrrhini). Am J Primatol 49:133–152
O’Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, Stanyon R, Copeland NG, Jenkins NA, Womack JE, Graves JAM (1999) The promise of comparative genomics in mammals. Science 286:458–481
Ovchinnikov I, Troxel AB, Swergold GD (2001) Genomic characterization of recent human LINE-1 insertions: evidence supporting random insertion. Genome Res 11:2050–2058
Parish DA, Vise P, Wichman HA, Bull JJ, Baker RJ (2002) Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 96:191–197
Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE (2011) A molecular phylogeny of living primates. PLos Genet 7:e1001342
Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci 83:2934–2938
Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositiong in mammals. Heredity 108:59–67
Röhe F (2006) Área de contato entre as distribuições geográficas de Saguinus midas e Saguinus bicolor (Callitrichidae-Primates): a importância de interações e fatores ecológicos. Master Thesis. Instituto Nacional de Pesquisa da Amazônia. Manaus, Amazonas
Rylands AB, Anzenberger G (2012) Introduction: New World primates. Int Zoo Yearb 46:4–10
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, pp 633–664
Santos WG (2005) Genética das populações do sauim-de-coleira (Saguinus bicolor - Callitrichidae) em fragmentos florestais e floresta contínua: implicações para conservação. Dissertação de Mestrado. Instituto Nacional de Pesquisa do Amazonas, Manaus, Amazonas
Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46:439–450
Subirá RJ (1998) Avaliação da situação atual das populações selvagens do sauim-de-coleira, Saguinus bicolor (Spix, 1823). Master Thesis. Universidade de Brasília. DF, Brasil
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 74:304–306
Sumner AT (1990) Chromosome Banding. Unwin Hyman Ltd., London
Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280–294
Waters PD, Dobigny G, Pardini AT, Robinson TJ (2004) LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes. Chromosoma 113:137–144
Xing J, Witherspoon DJ, Ray DA, Batzer MA, Jorde LB (2007) Mobile DNA elements in primate and human evolution. Anthroopology 50:2–19
Acknowledgements
This work was supported by the Universidade Federal do Amazonas (UFAM), Rede BioPHAM (CNPq/FAPEAM Grant No. 563348/2010-0); Pro-Amazon program on Biodiversity and Sustainability research (Proposal No. 047/2012); CAPES (Process 23038.009447/2013-45, Grant No. 3295/2013), FAPEAM (PAPAC 020/2013 and FIXAM 17/2014) and CNPq (process 482996/2011-0 and 476292/2013-1). CHS and DMBS received funding from CAPES and FAPEAM.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Serfaty, D.M.B., Carvalho, N.D.M., Gross, M.C. et al. Differential chromosomal organization between Saguinus midas and Saguinus bicolor with accumulation of differences the repetitive sequence DNA. Genetica 145, 359–369 (2017). https://doi.org/10.1007/s10709-017-9971-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-017-9971-0