Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 to Determine the Number and Topology of Horns in Bovidae

Author:

Allais-Bonnet Aurélie,Hintermann Aurélie,Deloche Marie-Christine,Cornette RaphaëlORCID,Bardou PhilippeORCID,Naval-Sanchez Marina,Pinton Alain,Haruda Ashleigh,Grohs Cécile,Zakany Jozsef,Bigi Daniele,Medugorac Ivica,Putelat Olivier,Greyvenstein Ockert,Hadfield Tracy,Ben Jemaa Slim,Bunevski Gjoko,Menzi Fiona,Hirter Nathalie,Paris Julia M.,Hedges John,Palhiere Isabelle,Rupp RachelORCID,Lenstra Johannes A.ORCID,Gidney Louisa,Lesur Joséphine,Schafberg Renate,Stache Michael,Wandhammer Marie-Dominique,Arbogast Rose-Marie,Guintard Claude,Blin Amandine,Boukadiri Abdelhak,Riviere Julie,Esquerré Diane,Donnadieu Cécile,Danchin-Burge Coralie,Reich Coralie M,Riley David,van Marle-Koster Este,Cockett Noelle,Hayes Benjamin J.,Drögemüller Cord,Kijas James,Pailhoux Eric,Tosser-Klopp Gwenola,Duboule DenisORCID,Capitan Aurélien

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

Cold Spring Harbor Laboratory

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