Centromere repositioning explains fundamental number variability in the New World monkey genus Saimiri

Abstract

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.

X Chromosome Evolution in Cetartiodactyla

“…It is likely that centromere repositioning (shift) or so-called evolutionary new centromere phenomenon, reflecting a change of centromere position on the chromosome without a change in the gene order, also occurred in cetartiodactyl X chromosome evolution. So far it was shown only in primates, rodents and perissodactyls [ 14 , 15 , 16 , 17 ].…”

Characterization of Satellite DNAs in Squirrel Monkeys genus Saimiri (Cebidae, Platyrrhini)

“…5). Variable FNs among squirrel monkey species is due to centromere repositioning in pairs 5 and 15 12 . Our sample includes specimens with both morphologies of chromosomes 5 and 15 and the alpha satDNA was always detected at their centromeres, indicating that these evolutionary new centromeres (ENCs) are mature.…”

Does the chromosomal position of 35S rDNA sites influence their transcription? A survey on Nothoscordum species (Amaryllidaceae)

“…The origin of Ap sites has been associated to different chromosomal rearrangements, such as centric fission, pericentric inversion, translocation and centromeric repositioning (Schubert and Lysak, 2011;Souza et al, 2016;Chiatante et al, 2017). Once established in the Ap position, 35S rDNA sites may take their advantage from their neighborhood, sandwiched between the pericentromeric and telomeric/subtelomeric heterochromatins, which would protect the protein coding genes close to NOR against an eventual propagation of the intense transcriptional activity of rDNA genes (McStay, 2016).…”