Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species

Abstract

Birds display remarkable diversity in the distribution and morphology of scales and feathers on their feet, yet the genetic and developmental mechanisms governing this diversity remain unknown. Domestic pigeons have striking variation in foot feathering within a single species, providing a tractable model to investigate the molecular basis of skin appendage differences. We found that feathered feet in pigeons result from a partial transformation from hindlimb to forelimb identity mediated by cis-regulatory changes in the genes encoding the hindlimb-specific transcription factor Pitx1 and forelimb-specific transcription factor Tbx5. We also found that ectopic expression of Tbx5 is associated with foot feathers in chickens, suggesting similar molecular pathways underlie phenotypic convergence between these two species. These results show how changes in expression of regional patterning genes can generate localized changes in organ fate and morphology, and provide viable molecular mechanisms for diversity in hindlimb scale and feather distribution.DOI: http://dx.doi.org/10.7554/eLife.12115.001

Flight feather development: its early specialization during embryogenesis

“…There are some mutants (strains) of domestic chickens and pigeons that have flight feather-like asymmetrical feathers in the hindlimb. Domyan et al [33] found that this intriguing phenotype is associated with cis -regulatory changes in the tbx5 locus that give rise to ectopic expression of tbx5 in the hindlimb bud, suggesting a role of this gene in flight feather formation.…”

“…Shh, a secretory molecule responsible for polarizing activity of the zone, also induces posterior feather buds when applied to the anterior margin [44]. Furthermore, ectopic flight feathers in pigeon and chicken mutants are biased to the posterior foot, and ectopic expression of tbx5 in the hindlimb in these mutants is also posterior-biased [33, 45]. Taken together with the fact that flight feathers in the raptor hindlimbs are also posterior-biased [30], it is thought that molecular networks for forelimb identity and posterior identity of the limb morphology coordinate formation of the FFF region.…”

Pigeonetics takes flight: Evolution, development, and genetics of intraspecific variation

“…Previous studies of chicken development and genetics suggest changes in dermal-epidermal interactions as a mechanism governing the decision between scaled and feathered epidermis (Chang et al, 2004; Crowe et al, 1998; Dorshorst et al, 2010; Harris et al, 2002; Harris et al, 2004; Somes, 1992; Zou and Niswander, 1996). Recent findings about the molecular basis of epidermal variation in pigeons, however, suggest a more fundamental developmental basis (Domyan et al, 2016). …”

“…The rock pigeon now has a high-quality reference genome, additional re-sequenced genomes representing a wide variety of breeds (NCBI Bioproject PRJNA284526), a catalog of over 25 million SNPs and genomic structural variants across breeds, and a draft genome-wide linkage map (Domyan et al, 2014; Domyan et al, 2016; Shapiro et al, 2013). These extensive resources, combined with standard experimental techniques developed for canonical model systems, make the pigeon a viable model to understand the genetic basis of phenotypic variation, and to test the developmental consequences of these genetic variants in developing embryos.…”

Regulatory evolution of Tbx5 and the origin of paired appendages

“…However, data on the expression of Tbx4/5 is sparse in jawless vertebrates (13-16, 18, 23, 24), and detailed comparative expression analysis in taxa with and without paired appendages is lacking. Moreover, whereas it has been hypothesized that cis-regulatory changes of Tbx5 have played an important role in pectoral fin evolution, an understanding of Tbx5 regulation is limited to amniotes and, therefore, lacking in more basal outgroups (15,(24)(25)(26)(27)(28).…”