Centromere repositioning explains fundamental number variability in the New World monkey genus Saimiri
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Cytogenetics has historically played a key role in research on squirrel monkey (genus Saimiri) evolutionary biology. Squirrel monkeys have a diploid number of 2n = 44, but vary in fundamental number (FN). Apparently, differences in FN have phylogenetic implications and are correlated with geographic regions. A number of hypothetical mechanisms were proposed to explain difference in FN: translocations, heterochromatin, or, most commonly, pericentric inversions. Recently, an additional mechanism, centromere repositioning, was discovered, which can alter chromosome morphology and FN. Here, we used chromosome banding, chromosome painting, and BAC-FISH to test these hypotheses. We demonstrate that centromere repositioning on chromosomes 5 and 15 is the mechanism that accounts for differences in FN. Current phylogenomic trees of platyrrhines provide a temporal framework for evolutionary new centromeres (ENC) in Saimiri. The X-chromosome ENC could be up to 15 million years (my) old that on chromosome 5 as recent as 0.3 my. The chromosome 15 ENC is intermediate, as young as 2.24 my. All ENC have abundant satellite DNAs indicating that the maturation process was fairly rapid. Callithrix jacchus was used as an outgroup for the BAC-FISH data analysis. Comparison with scaffolds from the S. boliviensis genome revealed an error in the last marmoset genome release. Future research including at the sequence level will provide better understanding of chromosome evolution in Saimiri and other platyrrhines. Probably other cases of differences in chromosome morphology and FN, both within and between taxa, will be shown to be due to centromere repositioning and not pericentric inversions.
KeywordsEvolutionary new centromeres Molecular cytogenetics Chromosome banding BAC-FISH Phylogenomics Chromosome rearrangements
The authors would like to thank the following persons for their assistance in obtaining and processing of specimens used in this study: Larisa S. Biltueva, Institute of Molecular and Cellular Biology, Novosibirsk; Camila do Nascimento Moreira and Yatiyo Yonenaga-Yassuda, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo; June Bellizzi (Assistant Director Zoological Affairs at Catoctin Zoo and Wildlife Preserve), and Richard Hahn (Director, Catoctin Zoo and Wildlife Preserve). This work was supported by PRIN (Progetti di Interesse Nazionale) to RS and by a grant from “Conselho Nacional de Desenvolvimento Cientifico e Tecnològico” (CNPq) to MS (process 407262/2013-0).
Compliance with ethical standards
No experimental protocols called for the handling of any animals because the cell lines used were kindly provided by individuals in other institutions.
Conflict of interest
The authors declare that they have no conflict of interests.
- Capozzi O, Archidiacono N, Lorusso N, Stanyon R, Rocchi M (2015) The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys. ChromosomaGoogle Scholar
- Carbone L, Nergadze SG, Magnani E, Misceo D, Francesca Cardone M, Roberto R, Bertoni L, Attolini C, Francesca Piras M, de Jong P, Raudsepp T, Chowdhary BP, Guerin G, Archidiacono N, Rocchi M, Giulotto E (2006) Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87:777–782CrossRefPubMedGoogle Scholar
- Lynch Alfaro JW, Boubli JP, Paim FP, Ribas CC, Silva MN, Messias MR, Rohe F, Merces MP, Silva Junior JS, Silva CR, Pinho GM, Koshkarian G, Nguyen MT, Harada ML, Rabelo RM, Queiroz HL, Alfaro ME, Farias IP (2015) Biogeography of squirrel monkeys (genus Saimiri): south-Central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol Phylogenet Evol 82(Pt B):436–454CrossRefPubMedGoogle Scholar
- Springer MS, Meredith RW, Gatesy J, Emerling CA, Park J, Rabosky DL, Stadler T, Steiner C, Ryder OA, Janečka JE, Fisher CA, Murphy WJ, Stanyon R (2012) Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS ONE 7(11):e49521. doi: 10.1371/journal.pone.0049521
- Stanyon R, Stone G (2008) Phylogenomic analysis by chromosome sorting and painting. Methods Mol Biol 422:13–29. doi: 10.1007/978-1-59745-581-7_2
- Yonenaga-Yassuda Y, Chu TH (1985) Chromosome banding patterns of Saimiri vanzolinii Ayres. Papiéis Avulsos de Zoologia, Museu de Zoologia da Universidade de São Paulo 36:165–168Google Scholar