Facial asymmetry tracks genetic diversity among Gorilla subspecies

Author:

McGrath Kate123ORCID,Eriksen Amandine B.4,García-Martínez Daniel5ORCID,Galbany Jordi36ORCID,Gómez-Robles Aida7,Massey Jason S.8,Fatica Lawrence M.39,Glowacka Halszka10,Arbenz-Smith Keely11,Muvunyi Richard12,Stoinski Tara S.13,Cranfield Michael R.14,Gilardi Kirsten14,Shalukoma Chantal15,de Merode Emmanuel15,Gilissen Emmanuel1617,Tocheri Matthew W.181920,McFarlin Shannon C.319,Heuzé Yann2

Affiliation:

1. State University of New York, College at Oneonta, Oneonta, NY 13820, USA

2. Univ. Bordeaux, CNRS, MC, PACEA, UMR 5199, 33615, Pessac, France

3. Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052, USA

4. Department of Biology, University of Indianapolis, 46227, USA

5. Physical Anthropology Unit, Department of Biodiversity, Ecology, and Evolution, Faculty of Biological Sciences, Complutense University of Madrid, Madrid, Spain

6. Department of Clinical Psychology and Psychobiology, University of Barcelona, Passeig de la Vall d'Hebron 171, 08035 Barcelona, Spain

7. Department of Anthropology, University College London, 14 Taviton St, London WC1H 0BW, UK

8. Department of Anatomy and Developmental Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia

9. Department of Physiological Sciences, University of Florida College of Veterinary Medicine, Gainesville, FL, USA

10. Department of Basic Medical Sciences, University of Arizona College of Medicine-Phoenix, Phoenix 85004, USA

11. Department of Small Animal Clinical Sciences, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, VA 24061, USA

12. Department of Tourism and Conservation, Rwanda Development Board, Kigali, Rwanda

13. The Dian Fossey Gorilla Fund International, Atlanta, GA 30315, USA

14. Gorilla Doctors (MGVP, Inc.), Karen C. Drayer Wildlife Health Center, University of California Davis, Davis, CA 95616, USA

15. Institut Congolais pour la Conservation de la Nature, Virunga National Park, Rumangabo, Democratic Republic of Congo

16. Department of African Zoology, Royal Museum for Central Africa, Tervuren, Belgium

17. Laboratory of Histology and Neuropathology, Université Libre de Bruxelles, Brussels, Belgium

18. Department of Anthropology, Lakehead University, Thunder Bay, Ontario, Canada P7B 5E1

19. Human Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA

20. Australian Research Council Centre of Excellence for Australian Biodiversity and Heritage, University of Wollongong, Wollongong, New South Wales 2522, Australia

Abstract

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

Funder

Leakey Foundation

2010 Max Planck Research Award to Timothy G. Bromage endowed by the German Federal Ministry of Education and Research to the Max Planck Society and the Alexander von Humboldt Foundation

H2020 Marie Skłodowska-Curie Actions

Smithsonian Collections Care and Preservation Fund

Investments for the Future Programme IdEx Université de Bordeaux / GPR Human Past

National Geographic Society

SYNTHESYS Project http://www.synthesys.info/ which is financed by European Community Research Infrastructure Action under the FP7 "Capacities" Program

The Ohio State University President's Postdoctoral Scholar's Program

Division of Behavioral and Cognitive Sciences

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

Reference54 articles.

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2. Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

3. Preferences for Symmetry in Conspecific Facial Shape Among Macaca mulatta

4. A meta-analysis of the heritability of developmental stability

5. The heritability of chimpanzee and human brain asymmetry

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