Lauriane Cacheux

Background: Alpha satellites, a superfamily of AT-rich tandem repeats, are the primary DNA component of centromeres in Platyrrhini and Catarrhini. Analyses of the human genome suggest that centromeres behave like biological ridges, with new alpha satellite families expanding at the centromere core, splitting and displacing older ones towards the pericentromeres. The Cercopithecini tribe, which displays an unusual chromosomal evolution involving multiple chromosomal fissions and centromere formations, represents a promising model to enhance our understanding of alpha satellite DNA evolutionary history. We previously applied targeted sequencing to centromere DNA from two distant species drawn from the Cercopithecini terrestrial and arboreal lineages, and characterized six alpha satellite families exhibiting varying mean sequence identities. Methods: Combining classical and molecular cytogenetics, we mapped the chromosomal distribution of these alpha satellite families across 13 Cercopithecini, one Papionini, and one Colobinae species. A nuclear marker-based phylogeny provided an evolutionary framework for interpretation. Results: Our phylogeny identifies the terrestrial and arboreal lineages, and a newly designated ‘swamp clade’. We observed significant interspecies variations in alpha satellite patterns, including differences in presence/absence and distinct chromosomal distribution patterns (centromeric, pericentromeric, or subtelomeric). Families previously described as heterogeneous (83–87% mean sequence identity) exhibit a centromeric position in the swamp lineage, which is characterized by conserved karyotypes. In contrast, these families show a pericentromeric distribution in the terrestrial and arboreal lineages, replaced at the centromere core by more homogeneous families (95–98% mean sequence identity). In the arboreal clade, which is characterized by highly fissioned karyotypes, putative evolutionary new centromeres show a unique co-occurrence of highly homogeneous and heterogeneous families. Conclusion & Implications: We propose a comprehensive evolutionary scenario for alpha satellite DNA in Cercopithecini, where younger families arise at the centromere core, shift toward the pericentromeres as they age, and eventually face extinction. Our study suggests that alpha satellite DNA and chromosomes evolve in an interdependent manner, with satellite diversification and displacement occurring in parallel with chromosome fissions and centromere repositioning. This comparative cytogenomic approach provides both support for the human-based evolutionary model for alpha satellite DNA and novel temporal insights into its diversification dynamics. Beyond evolutionary genomics, our findings highlight the potential of alpha satellite DNA to complement systematic studies in deciphering complex primate evolutionary histories.

Reticulate evolution is considered a widespread phenomenon in primates, as hybridization shaped evolutionary histories in all primate radiations, including Catarrhini. While genomic data suggest extensive ancient introgression among guenon lineages (tribe Cercopithecini), field and related genetic studies report extant hybridizations, along with fertility of guenon hybrids. By combining classical and molecular cytogenomics, we characterized chromosome organization for 12 guenon individuals, belonging to three species that associate in polyspecific groups: Cercopithecus cephus, C. nictitans and C. pogonias. Our results reveal multiple chromosomal heterozygosities in both the morphology of metaphase chromosomes and the molecular structure of centromeres, suggesting that chromosomal heterozygosity may be common in guenon genomes. Furthermore, we found similar chromosomal polymorphisms, involving similar chromosome and centromere variants, in distinct species. Our cytogenomic analysis also confirmed the hybrid origin of three individuals: two F1 hybrids between C. cephus and C. nictitans, and one backcross hybrid C. nictitans x (C. cephus x C. nictitans). Together, our results provide further possible evidence for reticulate evolution and incomplete reproductive isolation, and identify guenons as a good system to untangle the evolutionary dynamics of primate centromeres. This study provides a foundation for future research regarding the influence of hybridization on chromosomal reorganization, reproductive isolation, and speciation.