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.
Highlights
In birds, the genetic and developmental mechanisms that control the decision between scale and feather development remain poorly understood
Using quantitative trait locus (QTL) mapping with 130 F2 offspring genotyped at 3803 polymorphic markers (Broman et al, 2003), we identified two linkage groups (LG11 and LG20) that had significant effects on three different aspects of foot feathering (log10 odds ratio (LOD) > 4.6; Figure 1B–G, Table 1)
We examined expression of additional genes within the two candidate regions at Hamburger-Hamilton stage 25 (HH25), and found that the Tbx5 paralog Tbx3 was differentially expressed in both feather-footed pigeon breeds relative to racing homer (Figure 3—figure supplement 1B)
Summary
The genetic and developmental mechanisms that control the decision between scale and feather development remain poorly understood. Most birds possess scales on the foot (tarsometatarsus and toes) and feathers elsewhere. Exceptions to this pattern can provide insights into the evolutionary and developmental basis of skin appendage diversity. Some raptors and boreal birds evolved foot feathers instead of scales (’ptilopody’; Danforth, 1919; Lucas and Stettenheim, 1972), but the lack of appendage variation within these species precludes their use as genetic models. Most breeds have feet covered by scaled epidermis (wild-type), but scales are replaced by small feathers in grouse (gr) mutants, and by larger feather ’muffs’ in birds that carry mutant alleles at the Slipper (Sl) locus
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