Parallel genetic origin of foot feathering in birds

Understanding the genetic basis of similar phenotypes shared between lineages is a long-lasting research interest. Even though animal evolution offers many examples of parallelism, for many phenotypes little is known about the underlying genes and mutations. We here use a combination of whole-genome sequencing, expression analyses, and comparative genomics to study the parallel genetic origin of ptilopody (Pti) in chicken. Ptilopody (or foot feathering) is a polygenic trait that can be observed in domesticated and wild avian species and is characterized by the partial or complete development of feathers on the ankle and feet. In domesticated birds, ptilopody is easily selected to fixation, though extensive variation in the type and level of feather development is often observed. By mean of a genome-wide association analysis, we identified two genomic regions associated with ptilopody. At one of the loci, we identified a 17 kb deletion affecting PITX1 expression, a gene known to encode a transcription regulator of hindlimb identity and development. Similarly to pigeon, at the second loci we observed ectopic expression of TBX5, a gene involved in forelimb identity and a key determinant of foot feather development. We also observed that the trait evolved only once as foot feathered birds share the same haplotype upstream TBX5. Our findings indicate that in chicken and pigeon ptilopody is determined by the same set of genes that affect similar molecular pathways. Our study confirms that ptilopody has evolved through parallel evolution in chicken and pigeon.

解析不同支系间共有的相似表型的遗传基础，是学界长期以来的研究热点。尽管动物演化中存在诸多平行演化的实例，但针对多数表型，其背后的基因与突变机制仍不甚明晰。我们在此结合全基因组测序、表达分析与比较基因组学手段，研究家鸡中羽趾症（ptilopody, Pti）的平行遗传起源。羽趾症（又称足部羽化）是一种多基因性状，可在驯养与野生鸟类中观测到，其特征为脚踝与足部部分或完全发育出羽毛。在驯养鸟类中，羽趾症性状易于被选择至固定状态，但常可见羽毛发育类型与程度的广泛差异。通过全基因组关联分析，我们鉴定出两个与羽趾症相关的基因组区域。其中一个位点上，我们发现了一段17kb的缺失变异，该变异会影响PITX1的表达——PITX1是已知的编码后肢身份与发育调控转录因子的基因。与鸽子的研究情况类似，在第二个位点上，我们观测到TBX5的异位表达：TBX5参与前肢身份调控，是足部羽毛发育的关键决定因子。我们还发现，足部带羽的鸟类在TBX5上游共享同一单倍型，表明该性状仅演化出现过一次。我们的研究结果表明，家鸡与鸽子中的羽趾症均由影响相似分子通路的同一组基因所调控。本研究证实，家鸡与鸽子的羽趾症均通过平行演化途径产生。