More Than Skin Deep: Limb Identity and the Origins of Feathered Feet in Domestic Pigeons

The rock pigeon (Columba livia) is among the most phenotypically diverse and widely distributed avian species in the world. We are combining traditional genetics, whole-genome sequencing, and developmental analyses to understand the evolution of diversity among the hundreds of breeds within this species. In doing so, we are addressing fundamental questions about the genetic architecture of phenotypic change, including: How many genetic changes are required to yield pronounced anatomical changes? What are the identities of these key genes? What types of mutations underlie phenotypic variation (e.g., coding versus regulatory)? How do different loci interact to produce complex traits? Do similar traits in different breeds evolve via similar or different genetic mechanisms? In particular, our combined approach is revealing a spectrum of mutations that control the orientation, color, and placement of plumage within and among breeds. In one dramatic example, genome sequencing across breeds revealed variation at two key limb genes that was associated with the replacement of scales by feathers on the feet. Laboratory crosses and developmental studies showed that cis-regulatory changes in these genes interact to produce complex epidermal appendage variation. These epidermal changes, combined with alterations in muscle patterning and skeletal morphology, represent a partial homeotic shift in the hindlimb to a more forelimb-like identity. The genomics era is driving new discoveries about the molecular basis of diversity in non-traditional model organisms. The domestic pigeon is a promising model with which to explore the genetic architecture of derived, constructive phenotypes in a bird that is amenable to genetic, genomic, and developmental investigation.