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Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys

Christian Roos12*, Dietmar Zinner3, Laura S Kubatko4, Christiane Schwarz1, Mouyu Yang1, Dirk Meyer5, Stephen D Nash6, Jinchuan Xing7, Mark A Batzer8, Markus Brameier1, Fabian H Leendertz9, Thomas Ziegler5, Dyah Perwitasari-Farajallah10, Tilo Nadler11, Lutz Walter12 and Martin Osterholz112*

Author affiliations

1 Primate Genetics Laboratory, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

2 Gene Bank of Primates, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

3 Cognitive Ethology Laboratory, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

4 Departments of Statistics and Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, Ohio 43210, USA

5 Reproductive Biology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

6 Department of Anatomical Sciences, State University of New York, Stony Brook, New York 11794-8081, USA

7 Department of Human Genetics, University of Utah, 15 North 2030 East, Salt Lake City, Utah 84112, USA

8 Department of Biological Sciences, Louisiana State University, 202 Life Sciences Building, Baton Rouge, Louisiana 70803, USA

9 Research Group Emerging Zoonoses, Robert Koch Institute, Postfach 650261, 13302 Berlin, Germany

10 Primate Research Center and Department of Biology, Bogor Agricultural University, Jl. Lodaya II/5, Bogor 16151, Indonesia

11 Frankfurt Zoological Society, Endangered Primate Rescue Center, Cuc Phuong National Park, Nho Quan District, Ninh Binh Province, Vietnam

12 Stem Cell Biology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

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Citation and License

BMC Evolutionary Biology 2011, 11:77  doi:10.1186/1471-2148-11-77

Published: 24 March 2011



Colobine monkeys constitute a diverse group of primates with major radiations in Africa and Asia. However, phylogenetic relationships among genera are under debate, and recent molecular studies with incomplete taxon-sampling revealed discordant gene trees. To solve the evolutionary history of colobine genera and to determine causes for possible gene tree incongruences, we combined presence/absence analysis of mobile elements with autosomal, X chromosomal, Y chromosomal and mitochondrial sequence data from all recognized colobine genera.


Gene tree topologies and divergence age estimates derived from different markers were similar, but differed in placing Piliocolobus/Procolobus and langur genera among colobines. Although insufficient data, homoplasy and incomplete lineage sorting might all have contributed to the discordance among gene trees, hybridization is favored as the main cause of the observed discordance. We propose that African colobines are paraphyletic, but might later have experienced female introgression from Piliocolobus/Procolobus into Colobus. In the late Miocene, colobines invaded Eurasia and diversified into several lineages. Among Asian colobines, Semnopithecus diverged first, indicating langur paraphyly. However, unidirectional gene flow from Semnopithecus into Trachypithecus via male introgression followed by nuclear swamping might have occurred until the earliest Pleistocene.


Overall, our study provides the most comprehensive view on colobine evolution to date and emphasizes that analyses of various molecular markers, such as mobile elements and sequence data from multiple loci, are crucial to better understand evolutionary relationships and to trace hybridization events. Our results also suggest that sex-specific dispersal patterns, promoted by a respective social organization of the species involved, can result in different hybridization scenarios.