Past Connectivity but Recent Inbreeding in Cross River Gorillas Determined Using Whole Genomes from Single Hairs

Author:

Alvarez-Estape Marina1ORCID,Pawar Harvinder1ORCID,Fontsere Claudia12ORCID,Trujillo Amber E.34,Gunson Jessica L.34,Bergl Richard A.5,Bermejo Magdalena67,Linder Joshua M.8,McFarland Kelley9,Oates John F.10,Sunderland-Groves Jacqueline L.11,Orkin Joseph112ORCID,Higham James P.3,Viaud-Martinez Karine A.13ORCID,Lizano Esther114ORCID,Marques-Bonet Tomas1141516

Affiliation:

1. Institute of Evolutionary Biology (UPF-CSIC), PRBB, c/ del Dr. Aiguader 88, 08003 Barcelona, Spain

2. Center for Evolutionary Hologenomics, The Globe Institute, University of Copenhagen, Øster Farimagsgade 5A, 1352 Copenhagen, Denmark

3. Department of Anthropology, New York University, New York, NY 10003, USA

4. New York Consortium in Evolutionary Primatology, New York, NY 10065, USA

5. Conservation, Education and Science Department, North Carolina Zoo, Asheboro, NC 27205, USA

6. SPAC Scientific Field Station Network, Hasso Plattner Foundation (HPF), 14467 Potsdam, Germany

7. Department of Ecology and Environmental Sciences, University of Barcelona, 08028 Barcelona, Spain

8. Department of Anthropology, James Madison University, Harrisonburg, VA 22807, USA

9. Triton College, River Grove, IL 60171, USA

10. Department of Anthropology, Hunter College, City University of New York, New York, NY 10065, USA

11. Department of Forest Resources Management, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

12. Department of Anthropology, Montreal University, Montreal, QC H3T 1N8, Canada

13. Illumina Laboratory Services, Illumina Inc., 5200 Illumina Way, San Diego, CA 92122, USA

14. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Edifici ICTA-ICP, Cerdanyola del Vallès, 08193 Barcelona, Spain

15. Catalan Institution of Research and Advanced Studies (ICREA), Passeig de Lluís Companys, 23, 08010 Barcelona, Spain

16. CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Baldiri i Reixac 4, 08028 Barcelona, Spain

Abstract

The critically endangered western gorillas (Gorilla gorilla) are divided into two subspecies: the western lowland (G. g. gorilla) and the Cross River (G. g. diehli) gorilla. Given the difficulty in sampling wild great ape populations and the small estimated size of the Cross River gorilla population, only one whole genome of a Cross River gorilla has been sequenced to date, hindering the study of this subspecies at the population level. In this study, we expand the number of whole genomes available for wild western gorillas, generating 41 new genomes (25 belonging to Cross River gorillas) using single shed hairs collected from gorilla nests. By combining these genomes with publicly available wild gorilla genomes, we confirm that Cross River gorillas form three population clusters. We also found little variation in genome-wide heterozygosity among them. Our analyses reveal long runs of homozygosity (>10 Mb), indicating recent inbreeding in Cross River gorillas. This is similar to that seen in mountain gorillas but with a much more recent bottleneck. We also detect past gene flow between two Cross River sites, Afi Mountain Wildlife Sanctuary and the Mbe Mountains. Furthermore, we observe past allele sharing between Cross River gorillas and the northern western lowland gorilla sites, as well as with the eastern gorilla species. This is the first study using single shed hairs from a wild species for whole genome sequencing to date. Taken together, our results highlight the importance of implementing conservation measures to increase connectivity among Cross River gorilla sites.

Funder

Ministerio de Ciencia, Universidades e Investigación

Generalitat de Catalunya

European Research Council

AEI

NIH

Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya

Illumina Inc.

Government of Catalonia’s Secretariat for Universities and Research of the Ministry of Economy and Knowledge

“la Caixa” Foundation

European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement

Publisher

MDPI AG

Subject

Genetics (clinical),Genetics

Reference68 articles.

1. Guns, Germs, and Trees Determine Density and Distribution of Gorillas and Chimpanzees in Western Equatorial Africa;Strindberg;Sci. Adv.,2018

2. Dunn, A., Bergl, R., Byler, D., Eben-Ebai, S., Ndeloh Etiendem, D., Fotso, R., Ikfuingei, R., Imong, I., Jameson, C., and Macfie, L. (2014). Revised Regional Action Plan for the Conservation of the Cross River Gorilla (Gorilla gorilla diehli) 2014–2019, IUCN/SSC Primate Specialist Group and Wildlife Conservation Society.

3. Informing Conservation Management about Structural versus Functional Connectivity: A Case-Study of Cross River Gorillas;Imong;Am. J. Primatol.,2014

4. Remote Sensing Analysis Reveals Habitat, Dispersal Corridors and Expanded Distribution for the Critically Endangered Cross River Gorilla Gorilla gorilla diehli;Bergl;Oryx,2012

5. Oates, J., Sunderland-Groves, J., Bergl, R., Dunn, A., Nicholas, A., Takang, E., Omeni, F., Imong, I., Fotso, R., and Nkembi, L. (2007). Regional Action Plan for the Conservation of the Cross River Gorilla (Gorilla gorilla diehli), IUCN/SSC Primate Specialist Group and Wildlife Conservation Society.

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