Genomic Basis of Adaptive Divergence in Leg Length between Ground- and Tree-Dwelling Species within a Bird Family

Abstract

Hind limbs of tetrapods vary greatly in length and the variability can be associated with locomotor adaptation. Although the phenotypic evolution has been well documented, the underlying genetic basis remains poorly understood. We address this issue by integrating comparative genomics and functional prediction with a study system consisting of ground-dwelling, long-legged and tree-dwelling, short-legged species within the avian family Paridae. Genome-wide divergence and phenotypic correlation analyses jointly identified five highly divergent genomic regions that are significantly related with the difference in leg length between these two groups. Gene annotation for these regions detected three genes involved in skeletal development, that is, PTPA, BRINP1, and MIGA2, with the first one being under the strongest selection. Furthermore, four single nucleotide polymorphisms (SNPs) in the coding region of PTPA can well distinguish the two groups with distinct leg length. Among the four SNPs, one is non-synonymous mutation, and according to the prediction for protein structure and function, it can affect the 3D structure of the encoded protein by altering the corresponding amino acid's position. The alleles of PTPA were found in all sequenced species of the orders Palaeognathae and Psittaciformes, which typically take a ground locomotion style. A whole-genome scanning across bird species uncovered that the four SNPs are more likely to be present in resident passerines with increased leg length/wing length ratios (a proxy of leg-dependent locomotion efficiency). Our findings provide insight into the molecular evolution of locomotion performance based on leg morphology in birds.