A chromosome-level genome assembly of the Asian house martin implies potential genes associated with the feathered-foot trait

Abstract

The presence of feathers is a vital characteristic among birds, yet most modern birds had no feather on their feet. The discoveries of feathers on the hind limbs of basal birds and dinosaurs have sparked an interest in the evolutionary origin and genetic mechanism of feathered feet. However, the majority of studies investigating the genes associated with this trait focused on domestic populations. Understanding the genetic mechanism underpinned feathered-foot development in wild birds is still in its infancy. Here, we assembled a chromosome-level genome of the Asian house martin (Delichon dasypus) using the long-read High Fidelity sequencing approach to initiate the search for genes associated with its feathered feet. We employed the whole-genome alignment of D. dasypus with other swallow species to identify high-SNP regions and chromosomal inversions in the D. dasypus genome. After filtering out variations unrelated to D. dasypus evolution, we found six genes related to feather development near the high-SNP regions. We also detected three feather development genes in chromosomal inversions between the Asian house martin and the barn swallow genomes. We discussed their association with the wingless/integrated (WNT), bone morphogenetic protein, and fibroblast growth factor pathways and their potential roles in feathered-foot development. Future studies are encouraged to utilize the D. dasypus genome to explore the evolutionary process of the feathered-foot trait in avian species. This endeavor will shed light on the evolutionary path of feathers in birds.

Keywords: Asian house martin; Hi-C; PacBio Hifi; chromosome-level genome assembly; feathered feet; ptilopody.

Fig. 1.

a) The Asian house martin (D. dasypus). b) The Hi-C heatmap of the D. dasypus assembly displays 31 chromosome-level scaffolds. The gradient of darkness indicates the contact frequency of two points, with darker indicating higher frequencies of contacts. c) The phylogenetic relationship and the sequence divergence rate of four swallow species inferred from minimap2. The diagrams display the D-genies dot plot of whole-genome alignment of each swallow species against D. dasypus. The x-axis indicates the chromosomes of the Asian house martin genome, while the y-axis indicates the scaffolds of the other swallow genome assemblies. The line along the diagonal suggests high synteny between house martin scaffolds and barn swallow chromosomes with high sequence identity (>75%). Photo credit: Chih-Ming Hung.

Fig. 2.

Genetic divergence (Δ_SNP) between D. dasypus and three other swallow genomes. The Δ_SNP values of 10,000 bp windows are shown across the D. dasypus genome. Each panel indicates the result from the alignment of the D. dasypus genome with three swallow species (a) H. rustica; (b) R. riparia; (c) T. bicolor. In each panel, distinct color regions represent a corresponding chromosome in H. rustica, with a total of 35 chromosomes being considered. Each label on the x-axis consisted of three components: ChrN1-N2-N3, where N1, N2, and N3 represent three numbers. The first component, ChrN1, designates the respective chromosome in H. rustica to which D. dasypus is aligned. The second component, N2, signifies the original scaffold number in the D. dasypus genome. The third component, N3, denotes the window ID within the corresponding scaffold.

Fig. 3.

a) The Venn diagram illustrates the intersections of windows identified with top 1% Δ_SNP values between D. dasypus and each of the other three swallow species. STRING protein–protein interactions of (b) NBL1 and (c) GREM1. The colors of lines among proteins indicate types of protein–protein association.