Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae

Author:

Allais-Bonnet Aurélie123,Hintermann Aurélie4,Deloche Marie-Christine123,Cornette Raphaël5,Bardou Philippe67,Naval-Sanchez Marina8,Pinton Alain6,Haruda Ashleigh9,Grohs Cécile10,Zakany Jozsef4,Bigi Daniele11,Medugorac Ivica12,Putelat Olivier1314,Greyvenstein Ockert15,Hadfield Tracy16,Jemaa Slim Ben17,Bunevski Gjoko18,Menzi Fiona19,Hirter Nathalie19,Paris Julia M19,Hedges John20,Palhiere Isabelle6,Rupp Rachel6,Lenstra Johannes A21,Gidney Louisa22,Lesur Joséphine23,Schafberg Renate9,Stache Michael9,Wandhammer Marie-Dominique24,Arbogast Rose-Marie25,Guintard Claude2627,Blin Amandine28,Boukadiri Abdelhak10,Rivière Julie1029,Esquerré Diane30,Donnadieu Cécile30,Danchin-Burge Coralie31,Reich Coralie M32,Riley David G15,Marle-Koster Este van33,Cockett Noelle16,Hayes Benjamin J34,Drögemüller Cord19,Kijas James8,Pailhoux Eric23,Tosser-Klopp Gwenola6ORCID,Duboule Denis43536,Capitan Aurélien110ORCID

Affiliation:

1. ALLICE, Paris, France

2. Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas, France

3. Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort, France

4. Department of Genetics and Evolution, University of Geneva, Geneva, Switzerland

5. Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France

6. GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet-Tolosan, France

7. INRAE, Sigenae, Castanet-Tolosan, France

8. CSIRO Agriculture & Food, St. Lucia, QLD, Australia

9. Central Natural Science Collections, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany

10. Université Paris-Saclay, INRAE, AgroParisTech, GABI, Jouy-en-Josas, France

11. Dipartimento di Scienza e Tecnologie Agro-Alimentari, Alma Mater Studiorum University of Bologna, Bologna, Italy

12. Population Genomics Group, Department of Veterinary Sciences, Ludwig-Maximilians-University Munich, Munich, Germany

13. Archéologie Alsace, Sélestat, France

14. UMR 7044, ARCHIMEDE, MISHA, Strasbourg, France

15. Department of Animal Science, Texas A&M University, College Station, TX, USA

16. Department of Animal, Dairy, and Veterinary Sciences, Utah State University, Logan, UT, USA

17. Laboratoire des Productions Animales et Fourragères, Institut National de la Recherche Agronomique de Tunisie, Université de Carthage, Ariana, Tunisia

18. Livestock Department, Faculty of Agricultural Sciences and Food Institute of Animal Biotechnology, University Ss. Cyril and Methodius, Skopje, North Macedonia

19. Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland

20. Manx Loaghtan Sheep Breeders’ Group, Bassingbourn, Cambridgeshire, United Kingdom

21. Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands

22. Rent a Peasant, Tow Law, Bishop Auckland, Durham County, United Kingdom

23. Unité Archéozoologie, Archéobotanique, Sociétés Pratiques et Environnements (AASPE), CNRS, Muséum National d’Histoire Naturelle, Paris, France

24. Musée Zoologique de Strasbourg, Strasbourg, France

25. CNRS UMR 7044, ARCHIMEDE, MISHA, Strasbourg, France

26. Unité d’Anatomie Comparée, Ecole Nationale Vétérinaire de l’Agroalimentaire et de l’Alimentation, Nantes Atlantique—ONIRIS, Nantes, France

27. Groupe d’Études Remodelage Osseux et bioMatériaux (GEROM), Université d’Angers, Unité INSERM 922, LHEA/IRIS-IBS, CHU d’Angers, Angers, France

28. Muséum National d’Histoire Naturelle, CNRS, UMS 2700 2AD, Paris, France

29. INRAE, Micalis Institute, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France

30. INRAE, US, 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France

31. Institut de l’Elevage, Paris, France

32. Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC, Australia

33. Department of Science, University of Pretoria, Hatfield, South Africa

34. Queensland Alliance for Agriculture and Food Innovation (QAAFI), Centre for Animal Science, University of Queensland, St. Lucia, QLD, Australia

35. Swiss Cancer Research Institute, EPFL, Lausanne, Switzerland

36. Collège de France, Paris, France

Abstract

Abstract In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. These results highlight the key role played by this gene in headgear patterning and illustrate the evolutionary co-option of a gene involved in the early development of bilateria to properly fix the position and number of these distinctive organs of Bovidae.

Publisher

Oxford University Press (OUP)

Subject

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

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