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Alpha satellite DNA is a major DNA component of primate centromeres. We previously reported that Azara's owl monkey has two types of alpha satellite DNA, OwlAlp1 and OwlAlp2. OwlAlp2 (344 bp) exhibits a sequence similarity throughout its entire length with alpha satellite DNA of closely related species. OwlAlp1 (185 bp) corresponds to the part of OwlAlp2. Based on the observation that the CENP-A protein binds to OwlAlp1, we proposed that OwlAlp1 is a relatively new repetitive DNA that replaced OwlAlp2 as the centromeric satellite DNA. However, a detailed picture of the evolutionary process of this centromere DNA replacement remains largely unknown. Here, we performed a phylogenetic analysis of OwlAlp1 and OwlAlp2 sequences, and also compared our results to alpha satellite DNA sequences of other primate species. We found that: (i) OwlAlp1 exhibits a higher similarity to OwlAlp2 than to alpha satellite DNA of other species, (ii) OwlAlp1 has a single origin, and (iii) sequence variation is lower in OwlAlp1 than in OwlAlp2. We conclude that OwlAlp1 underwent a recent and rapid expansion in the owl monkey lineage. This centromere DNA replacement could have been facilitated by the heterochromatin reorganization that is associated with the adaptation of owl monkeys to a nocturnal lifestyle., (© 2021 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.)

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.

Most evolutionary new centromeres (ENC) are composed of large arrays of satellite DNA and surrounded by segmental duplications. However, the hypothesis is that ENCs are seeded in an anonymous sequence and only over time have acquired the complexity of "normal" centromeres. Up to now evidence to test this hypothesis was lacking. We recently discovered that the well-known polymorphism of orangutan chromosome 12 was due to the presence of an ENC. We sequenced the genome of an orangutan homozygous for the ENC, and we focused our analysis on the comparison of the ENC domain with respect to its wild type counterpart. No significant variations were found. This finding is the first clear evidence that ENC seedings are epigenetic in nature. The compaction of the ENC domain was found significantly higher than the corresponding WT region and, interestingly, the expression of the only gene embedded in the region was significantly repressed., Competing Interests: E.E.E. is on the scientific advisory board (SAB) of DNAnexus and is a consultant for Kunming University of Science and Technology (KUST) as part of the 1000 China Talent Program.

Molecular cytogenetics provides a visual, pictorial record of the tree of life, and in this respect the fusion origin of human chromosome 2 is a well-known paradigmatic example. Here we report on a variant chromosome 6 in which the centromere jumped to 6p22.1. ChIP-chip experiments with antibodies against the centromeric proteins CENP-A and CENP-C exactly defined the neocentromere as lying at chr6:26,407-26,491 kb. We investigated in detail the evolutionary history of chromosome 6 in primates and found that the primate ancestor had a homologous chromosome with the same marker order, but with the centromere located at 6p22.1. Sometime between 17 and 23 million years ago (Mya), in the common ancestor of humans and apes, the centromere of chromosome 6 moved from 6p22.1 to its current location. The neocentromere we discovered, consequently, has jumped back to the ancestral position, where a latent centromere-forming potentiality persisted for at least 17 Myr. Because all living organisms form a tree of life, as first conceived by Darwin, evolutionary perspectives can provide compelling underlying explicative grounds for contemporary genomic phenomena.

The centromere has a pivotal role in structuring chromosomal architecture, but remains a poorly understood and seemingly paradoxical "black hole." Centromeres are a very rapidly evolving segment of the genome and it is now known that centromere shifts in evolution are not rare and must be considered on a par with other chromosome rearrangements. Recently, unprecedented findings on neocentromeres and evolutionary new centromeres (ENC) have helped clarify the relationship of the centromere within the genome and shown that these two phenomena are two faces of the same coin. No prominent sequence features are known that promote centromere formation and both types of new centromeres are formed epigenetically, both clinical neocentromeres and ENC cluster at chromosomal "hotspots." The clustering of neocentromeres in 8p is probably the result of the relatively high frequency of noncanonical pairing. Studies on the evolution of the chromosomes 3, 13, and 15 help explain why there are clusters of neocentromeres. These domains often correspond to ancestral inactivated centromeres and some regions can preserve features that trigger neocentromere emergence over tens of millions of years. Neocentromeres may be correlated with the distribution of segmental duplications (SDs) in regions of extreme plasticity that often can be characterized as gene deserts. Further, because centromeres and associated pericentric regions are dynamically complex, centromere shifts may turbocharge genome reorganization by influencing the distribution of heterochromatin. The "reuse" of regions as centromere seeding-points in evolution and in human clinical cases further extends the concept of "reuse" of specific domains for "chromosomal events."

A systematic fluorescence in situ hybridization comparison of macaque and human synteny organization disclosed five additional macaque evolutionary new centromeres (ENCs) for a total of nine ENCs. To understand the dynamics of ENC formation and progression, we compared the ENC of macaque chromosome 4 with the human orthologous region, at 6q24.3, that conserves the ancestral genomic organization. A 250-kilobase segment was extensively duplicated around the macaque centromere. These duplications were strictly intrachromosomal. Our results suggest that novel centromeres may trigger only local duplication activity and that the absence of genes in the seeding region may have been important in ENC maintenance and progression.

Background: Evolutionary centromere repositioning and human analphoid neocentromeres occurring in clinical cases are, very likely, two stages of the same phenomenon whose properties still remain substantially obscure. Chromosome 13 is the chromosome with the highest number of neocentromeres. We reconstructed the mammalian evolutionary history of this chromosome and characterized two human neocentromeres at 13q21, in search of information that could improve our understanding of the relationship between evolutionarily new centromeres, inactivated centromeres, and clinical neocentromeres., Results: Chromosome 13 evolution was studied, using FISH experiments, across several diverse superordinal phylogenetic clades spanning >100 million years of evolution. The analysis revealed exceptional conservation among primates (hominoids, Old World monkeys, and New World monkeys), Carnivora (cat), Perissodactyla (horse), and Cetartiodactyla (pig). In contrast, the centromeres in both Old World monkeys and pig have apparently repositioned independently to a central location (13q21). We compared these results to the positions of two human 13q21 neocentromeres using chromatin immunoprecipitation and genomic microarrays., Conclusion: We show that a gene-desert region at 13q21 of approximately 3.9 Mb in size possesses an inherent potential to form evolutionarily new centromeres over, at least, approximately 95 million years of mammalian evolution. The striking absence of genes may represent an important property, making the region tolerant to the extensive pericentromeric reshuffling during subsequent evolution. Comparison of the pericentromeric organization of chromosome 13 in four Old World monkey species revealed many differences in sequence organization. The region contains clusters of duplicons showing peculiar features.

The genus Saimiri is a decades-long taxonomic and phylogenetic puzzle to which cytogenetics has contributed crucial data. All Saimiri species apparently have a diploid number of 2n = 44 but vary in the number of chromosome arms. Repetitive sequences such as satellite DNAs are potentially informative cytogenetic markers because they display high evolutionary rates. Our goal is to increase the pertinent karyological data by more fully characterizing satellite DNA sequences in the Saimiri genus. We were able to identify two abundant satellite DNAs, alpha (~340 bp) and CapA (~1,500 bp), from short-read clustering of sequencing datasets from S. boliviensis. The alpha sequences comprise about 1% and the CapA 2.2% of the S. boliviensis genome. We also mapped both satellite DNAs in S. boliviensis, S. sciureus, S. vanzolinii, and S. ustus. The alpha has high interspecific repeat homogeneity and was mapped to the centromeres of all analyzed species. CapA is associated with non-pericentromeric heterochromatin and its distribution varies among Saimiri species. We conclude that CapA genomic distribution and its pervasiveness across Platyrrhini makes it an attractive cytogenetic marker for Saimiri and other New World monkeys. [ABSTRACT FROM AUTHOR]

In the Cercopithecini ancestor two chromosomes, homologous to human chromosomes 20 and 21, fused to form the Cercopithecini specific 20/21 association. In some individuals from the genus Cercopithecus, this association was shown to be polymorphic for the position of the centromere, suggesting centromere repositioning events. We set out to test this hypothesis by defining the evolutionary history of the 20/21 association in four Cercopithecini species from three different genera. The marker order of the various 20/21 associations was established using molecular cytogenetic techniques, including an array of more than 100 BACs. We discovered that five different forms of the 20/21 association were present in the four studied Cercopithecini species. Remarkably, in the two Cercopithecus species, we found individuals in which one homolog conserved the ancestral condition, but the other homolog was highly rearranged. The phylogenetic analysis showed that the heterozygosity in these two species originated about 8 million years ago and was maintained for this entire arc of time, surviving multiple speciation events. Our report is a remarkable extension of Dobzhansky's pioneering observation in Drosophila concerning the maintenance of chromosomal heterozygosity due to selective advantage. Dobzhansky's hypothesis recently received strong support in a series of detailed reports on the fruit fly genome. Our findings are first extension to primates, indeed to Old World monkeys phylogenetically close to humans of an analogous situation. Our results have important implications for hypotheses on how chromosome rearrangements, selection, and speciation are related. [ABSTRACT FROM AUTHOR]