Genetic and Molecular Basis of Feather Diversity in Birds

Abstract

Feather diversity is striking in many aspects. Although the development of feather has been studied for decades, genetic and genomic studies of feather diversity have begun only recently. Many questions remain to be answered by multidisciplinary approaches. In this review, we discuss three levels of feather diversity: Feather morphotypes, intraspecific variations, and interspecific variations. We summarize recent studies of feather evolution in terms of genetics, genomics, and developmental biology and provide perspectives for future research. Specifically, this review includes the following topics: 1) Diversity of feather morphotype; 2) feather diversity among different breeds of domesticated birds, including variations in pigmentation pattern, in feather length or regional identity, in feather orientation, in feather distribution, and in feather structure; and 3) diversity of feathers among avian species, including plumage color and morph differences between species and the regulatory differences in downy feather development between altricial and precocial birds. Finally, we discussed future research directions.

Fig. 1.

—Different types of feather in a chicken. (A) Downy feather, contour feather, and flight feather. (B) Developing and mature embryonic and adult chicken feathers. The branches in downy feathers only include the ramus and barbules, whereas most adult chicken feathers are bilaterally symmetric and include a rachis, ramus, and barbules. (A) Adapted from Lucas and Stettenheim (1972). (B) Adapted from Ng et al. (2012).

Fig. 2.

—The genome size, numbers of α- and β-keratin genes, and keratinized skin appendages of amniotes. The phylogeny of amniotes is based on molecular studies (Hedges and Poling 1999; Shen et al. 2011; Tzika et al. 2011; Chiari et al. 2012; Hedges 2012). The genome sizes of mammals, lepidosaurs, turtles, crocodilians, non-avian theropods, and birds are presented as clade-wide averages based on recent genomic and paleontological studies (Organ et al. 2007; Janes et al. 2010). The numbers of α- and β-keratin genes are based on recent genomic or developmental studies on some representative species, such as American alligator (Alligator mississippiensis), saltwater crocodile (Crocodylus porosus), green sea turtle (Chelonia mydas), western painted turtle (Chrysemys picta belli), Chinese soft-shelled turtle (Pelodiscus sinensis), green anole lizard (Anolis carolinensis), human (Homo sapiens), and 48 species of birds (Dalla Valle et al. 2010; Greenwold et al. 2014; Holthaus et al. 2016). Although only three major feather morphotypes are shown here, dinosaurs and birds actually have diverse morphotypes of feather, such as monofilamentous, radially branched, bilaterally branched, symmetrical flight, and asymmetrical flight feathers (Xu et al. 2014; Chen et al. 2015).

Fig. 3.

—Schematic topographic representation of differentially expressed α- and β-keratin genes in skin appendages of embryo and adult chicken based on in situ hybridization and RNA-seq data. Colors represent particular α- and β-keratin genes in certain appendages. Upper panel: Regional differences among skin appendages. Middle panel: Intra-appendage differences in α- and β-keratin expression. Bottom panel: Chromosomal arrangements of β-keratin genes on Chr25 and Chr27. Claw, claw-β-keratin; FK, feather-β-keratin; FL, feather-like-β-keratin; Ktn, keratinocyte-β-keratin; Scale, scale-β-keratin. Adapted from Wu et al. (2015).

Fig. 4.

—Frizzle mutation. (A) Adult and 1-month-old frizzle chickens. (B) Comparison of body feathers of normal white leghorns and frizzle chickens in dorsal, ventral, and side views. (C) Upper panel: PCNA and TUNEL staining at different levels of the rachis. Lower panel: Top view of a cross section through the rachis in a pennaceous vane of body feathers. (D) Chicken KRT75 and the cryptic splicing site activated by the deletion that covers positions 224 of exon 5 to +59 of intron 5. Black boxes represent exon sequences; intron 5 is designated by a line. The caret designating use of the cryptic splicing site (position 269) is shown below, and the caret designating use of the authentic site is shown above the diagram of the pre-mRNA. (E) Partial sequence of the F allele of KRT75 gene. Light gray letters show the 84-bp deletion in genomic DNA. Dark gray letters show the additional deletion in exon 5 created by a cryptic splicing site. One transcript with a 69-bp deletion is produced by the activation of the cryptic splicing site. Therefore, a protein with a deletion of 23 amino acids (positions 311–333) may be produced. Capital and small letters show parts of exon 5 and intron 5, respectively. The authentic and cryptic mRNA splicing sites are demonstrated by the underlines. Adapted from Ng et al. (2012).

Fig. 5.

—Dorsal natal down formations in zebra finch and chicken. (A) Dorsal view of the feather tracts in a zebra finch hatchling. Open circles show feather buds that do not develop into downy feathers, and black circles indicate downy feather formations. (B) Type I (open circles) and type II (black circles) feather formations. Type I feather buds do not develop into downy feather, and contour feathers develop directly feather buds. In contrast, in the middle stripe of the posterior dorsal tract and other regions labeled with black circles, the feather buds form natal down before the growth of the contour feathers, same as the natal down formation process in chickens. (C) A summary diagram of types I and II feather formations, and genes involved in the down development pathway. Adapted from Chen et al. (2016).