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Eight million years of maintained heterozygosity in chromosome homologs of cercopithecine monkeys

  • Doron Tolomeo
  • Oronzo Capozzi
  • Giorgia Chiatante
  • Luca Sineo
  • Takafumi Ishida
  • Nicoletta Archidiacono
  • Mariano RocchiEmail author
  • Roscoe StanyonEmail author
Original Article


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.


Chromosomes Heterozygosity Primates Evolution Heterozygous advantage 



The authors would like to thank Lorenzo Parenti and Laura Eccel whose master theses at the University of Florence provided background information on CAL and CPE karyotypes and painting patterns. We thank Fengtang Yang for his supervision of Lorenzo Parenti during his Erasmus Placement stage at the Welcome Centre (Cambridge, UK) during which among other techniques, he learned and performed M-FISH on CPE and CAL metaphases. The authors thank Vito Ruffino (Bioparco di Sicilia) for the access to C. petaurista.

Funding information

This work was supported by PRIN (Progetti di Interesse Nazionale) research grant (grant number 2015RA7XZS), from the Italian Ministry of Education and University, to NA, MR, and RS.

Supplementary material

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© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of BiologyUniversity of FlorenceFlorenceItaly
  2. 2.Department of BiologyUniversity of BariBariItaly
  3. 3.Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e FarmaceuticheUniversità degli Studi di PalermoPalermoItaly
  4. 4.Department of Biological SciencesGraduate School of Science, University of TokyoTokyoJapan

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