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

Aurélie Allais‐Bonnet, Aurélie Hintermann, Marie-Christine Deloche, Raphaël Cornette, Philippe Bardou, Marina Naval-Sánchez, Alain Pinton, Ashleigh Haruda, Cécile Grohs, József Zákány, Daniele Bigi, Ivica Međugorac, Olivier Putelat, Ockert Greyvenstein, Tracy Hadfield, Slim Ben Jemaa, Gjoko Bunevski, Fiona Menzi, Nathalie Hirter, Julia M. Paris, John Hedges, Isabelle Palhière, Rachel Rupp, Johannes A. Lenstra, Louisa Gidney, Joséphine Lesur, Renate Schafberg, Michael Stache, Marie-Dominique Wandhammer, Rose‐Marie Arbogast, Claude Guintard, Amandine Blin, Abdelhak Boukadiri, Julie Rivière, Diane Esquerré, Cécile Donnadieu, Coralie Danchin-Burge, Coralie M. Reich, David G. Riley, E. van Marle-Köster, Noelle E. Cockett, Ben J. Hayes, Cord Drögemüller, James Kijas, Éric Pailhoux, Gwenola Tosser‐Klopp, Denis Duboule, Aurélien Capitan

2021Molecular Biology and Evolution33 citationsDOIOpen Access PDF

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.

Topics & Concepts

BiologyBilateriaBovidaeEvolutionary biologyAppendageGeneticsAlleleEvolutionary developmental biologyFrench hornGeneAnatomyPhylogeneticsZoologyPsychologyPedagogydental development and anomaliesPlant Taxonomy and PhylogeneticsGenetic and phenotypic traits in livestock