Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation

Author:

Jensen Axel1ORCID,Swift Frances2,de Vries Dorien3,Beck Robin M D3,Kuderna Lukas F K4,Knauf Sascha5,Chuma Idrissa S6,Keyyu Julius D7,Kitchener Andrew C89ORCID,Farh Kyle4,Rogers Jeffrey10ORCID,Marques-Bonet Tomas1112131415,Detwiler Kate M16,Roos Christian17,Guschanski Katerina12ORCID

Affiliation:

1. Department of Ecology and Genetics, Animal Ecology, Uppsala University , Uppsala SE-75236 , Sweden

2. School of Biological Sciences, Institute of Ecology and Evolution, University of Edinburgh , Edinburgh , UK

3. School of Science, Engineering & Environment, University of Salford , Salford M5 4WT , UK

4. Illumina Artificial Intelligence Laboratory, Illumina Inc. , Foster City, CA 94404 , USA

5. Institute of International Animal Health/One Health, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , Greifswald – Insel Riems 17493 , Germany

6. Tanzania National Parks , Arusha , Tanzania

7. Tanzania Wildlife Research Institute (TAWIRI) , Arusha , Tanzania

8. Department of Natural Sciences, National Museums Scotland , Edinburgh EH1 1JF , UK

9. School of Geosciences , University of Edinburgh, Edinburgh EH8 9XP , UK

10. Human Genome Sequencing Center and Department of Molecular and Human Genetics, Baylor College of Medicine , Houston, TX 77030 , USA

11. Institute of Evolutionary Biology (UPF-CSIC), PRBB , Barcelona 08003 , Spain

12. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona , Barcelona , Spain

13. Catalan Institution of Research and Advanced Studies (ICREA) , Barcelona , Spain

14. CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST) , Barcelona 08028 , Spain

15. Institució Catalana de Recerca i Estudis Avançats (ICREA) and Universitat Pompeu Fabra , Barcelona 08010 , Spain

16. Department of Biological Sciences, Florida Atlantic University , Boca Raton, FL , USA

17. Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research , Göttingen 37077 , Germany

Abstract

Abstract Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as an important evolutionary force. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world's largest primate radiations, we show that rampant gene flow characterizes their evolutionary history and identify ancient hybridization across deeply divergent lineages that differ in ecology, morphology, and karyotypes. Some hybridization events resulted in mitochondrial introgression between distant lineages, likely facilitated by cointrogression of coadapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproductive isolation. In line with reports from other systems that hybridization might facilitate diversification, we find that some of the most species-rich guenon clades are of admixed origin. This study provides important insights into the prevalence, role, and outcomes of ancestral hybridization in a large mammalian radiation.

Funder

Swedish Research Council

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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