Chimpanzee behavioural diversity is spatially structured and negatively associated with genetic variation

Author:

Barratt Christopher1ORCID,Gratton Paolo2,Marta Silvio3ORCID,Onstein Renske4,Fontsere Claudia5ORCID,Lester Jack6,Kalan Ammie7ORCID,Kulik Lars6,Bocksberger Gaelle8ORCID,Dieguez Paula6,McCarthy Maureen6,Kuhlwilm Martin9ORCID,Abwe Ekwoge10,Agbor Anthony6,Angedakin Samuel6,Assumang Alfred11,Aubert Floris12,Ayimisin Emmanuel6,Bailey Emma6,Barciela Amanda13,Barubiyo Donatienne6,Bessone Mattia6,Brazzola Gregory6,Buh Valentine Ebua6,Chancellor Rebecca14,Cohen Heather6,Corogenes Katherine6,Coupland Charlotte6,Danquah Emmanuel11ORCID,Deschner Tobias15,Dunn Andrew16,Dupain Jef17,Egbe Villard6,Granjon Anne-Céline6ORCID,Hedwig Daniela18,Hermans Veerle19,Hernandez-Aguilar R. Adriana20ORCID,Imong Inaoyom21,Jeffery Kathryn22ORCID,Jones Sorrel6ORCID,Junker Jesscia6,Kambere Mbangi6,Kambi Mohamed6,Kienast Ivonne6,Kujirakwinja Deo16,Langergraber Kevin23,Lapuente Juan6,Larson Bradley6,Lee Kevin24,Llana Manuel13,Martin Rumen6,Mbi Tanyi6,Meier Amelia6,Morgan Bethan25,Morgan David26,Neil Emily6ORCID,Nicholl Sonia27ORCID,Nixon Stuart28,Niyigaba Protais16,Normand Emmanuelle12,Orbell Christopher29,Ormsby Lucy6,Orume Robinson30,Pacheco Liliana31ORCID,Piel Alex32,Preece Jodie6,Robbins Martha6,Rundus Aaron14,Sanz Crickette33ORCID,Schijndel Joost van6,Sommer Volker34,Stewart Fiona34,Tagg Nikki35,Tédonzong Luc Roscelin19ORCID,Tickle Alexander6,Vendras Elleni6,Vergnes Virginie12,Vyalengerera Magloire6,Welsh Adam6,Wessling Erin36,Willie Jacob19,Wittig Roman37,Yuh Yisa Ginath6ORCID,Yurkiw Kyle6,Zuberbühler Klaus38,Andres Aida34,Marques-Bonet Tomas39ORCID,Boesch Christophe12,Arandjelovic Mimi40ORCID,Kühl Hjalmar41

Affiliation:

1. German Centre for Integrative Biodiversity Research

2. University of Rome “Tor Vergata”

3. University of Milan

4. Naturalis Biodiversity Center

5. The Globe Institute, University of Copenhagen

6. Max Planck Institute for Evolutionary Anthropology

7. University of Victoria

8. Senckenberg Biodiversity and Climate Research Centre

9. University of Vienna

10. Ebo Forest Research Project

11. Department of Wildlife and Range Management, Faculty of Renewable Natural Resources, Kwame Nkrumah University of Science and Technology

12. Wild Chimpanzee Foundation

13. Jane Goodall Institute Senegal

14. West Chester University

15. University of Osnabrück

16. Wildlife Conservation Society

17. ntwerp Zoo Foundation-KMDA, Royal Zoological Society of Antwerp

18. The Aspinall Foundation

19. Royal Zoological Society of Antwerp

20. University of Oslo

21. Wildlife Conservation Society (WCS)

22. University of Stirling

23. Arizona State University

24. University of Arizona

25. San Diego Zoo Wildlife Alliance

26. Lincoln Park Zoo

27. Parks Canada Agency

28. North of England Zoological Society, Chester Zoo,

29. Panthera

30. Korup Rainforest Conservation Society

31. WARA Conservation Project-GALF

32. UCL

33. Washington University

34. University College London

35. KMDA, Centre for Research and Conservation, Royal Zoological Society of Antwerp

36. Department of Human Evolutionary Biology, Harvard University

37. Bridge Researcher Evolution of Brain Connectivity (CNRS / MPS) , Institute for Cognitive Sciences Marc Jeannerod, UMR 5229 CNRS / University of Lyon

38. University of Neuchâtel

39. Institut de Biologia Evolutiva (CSIC/Universitat Pompeu Fabra) / CNAG (Centro de Analisis Genomico) PCB

40. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig

41. Senckenberg Museum für Naturkunde Görlitz

Abstract

Abstract The question of how behavioural diversity in humans and other animals is shaped by the combined influence of demography, genetics, culture, and the environment receives much research attention. We take a macro-ecological approach to evaluate how chimpanzee (Pan troglodytes) behavioural diversity is spatially structured and associated with genetic diversity (i.e. heterozygosity as a proxy for effective population size) and contemporary and historic environmental context. We integrate the largest available chimpanzee behavioural and genomic datasets and apply spatially explicit Bayesian Generalised Linear Mixed Models to derive marginal effects for putative drivers and range wide spatial predictions of probability to observe behavioural traits. Contrary to expectations from neutral models of behavioural evolution, we observed a negative association of genetic diversity with behavioural diversity. This result suggests that behavioural traits may impact fitness. In contrast, we observed weaker associations of chimpanzee behavioural diversity with contemporary and historic environmental context. The very strong spatial structuring of behavioural traits is consistent with cultural transmission playing a major role in shaping chimpanzee behavioural diversity. Our analytical approach can be flexibly extended by additional candidate drivers of chimpanzee behavioural diversity, and offers a novel framework for testing competing ecological-evolutionary hypotheses across a wide variety of animal cultures.

Publisher

Research Square Platform LLC

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