E-MTAB-6794
A role for differential gene regulation in the rapid diversification of melanic plumage coloration in the dark-eyed junco (Junco hyemalis)
Plumage color plays a prominent role in reproductive isolation and thus understanding the genetic basis of pigmentation patterns can provide critical insight into speciation. Subspecies of the dark-eyed junco (Junco hyemalis) show marked differences in melanic plumage coloration known to have evolved rapidly since the Last Glacial Maximum just 18,000 years ago. To understand this rapid radiation we studied the pigment composition and the genetic basis of coloration in two divergent subspecies, the slate-colored and Oregon juncos. We used HPLC and light microscopy to investigate pigment deposition patterns in feathers from four body areas. RNA-seq data generated under common garden experimental conditions were then used to compare the relative roles of differential gene expression in growing feathers and sequence divergence in loci expressed during feather development. Junco feathers were found to differ in eumelanin and pheomelanin content and distribution, producing a range of black, gray and brown colors. Transcriptomic data revealed marked regulatory differences among subspecies and among body-parts within subspecies in known melanin-pathway genes (including PMEL, TYR, TYRP1, OCA2, MLANA), but also in several novel or poorly known loci (EDAR, VPS33B, HPS1). Within subspecies, lighter feathers expressed less melanin synthesis genes, more ASIP, and showed differential expression of Wnt signaling genes. Feathers from different body regions also showed differential expression of Hox genes. The two subspecies differed in expression of ASIP and three other genes (MFSD12, KCNJ13, HAND2) previously associated with color development. Sequence variation in the expressed genes was not related to color differences between junco subspecies. Our findings suggest that differential expression of a few genes can account for marked differences in plumage color and pattern, a mechanism that can account for the rapid diversification of juncos. Several novel candidate pigmentation genes found in juncos may contribute to the expression of melanic coloration in other vertebrates.
Plumage color plays a prominent role in reproductive isolation and thus understanding the genetic basis of pigmentation patterns can provide critical insight into speciation. Subspecies of the dark-eyed junco (Junco hyemalis) show marked differences in melanic plumage coloration known to have evolved rapidly since the Last Glacial Maximum just 18,000 years ago. To understand this rapid radiation we studied the pigment composition and the genetic basis of coloration in two divergent subspecies, the slate-colored and Oregon juncos. We used HPLC and light microscopy to investigate pigment deposition patterns in feathers from four body areas. RNA-seq data generated under common garden experimental conditions were then used to compare the relative roles of differential gene expression in growing feathers and sequence divergence in loci expressed during feather development. Junco feathers were found to differ in eumelanin and pheomelanin content and distribution, producing a range of black, gray and brown colors. Transcriptomic data revealed marked regulatory differences among subspecies and among body-parts within subspecies in known melanin-pathway genes (including PMEL, TYR, TYRP1, OCA2, MLANA), but also in several novel or poorly known loci (EDAR, VPS33B, HPS1). Within subspecies, lighter feathers expressed less melanin synthesis genes, more ASIP, and showed differential expression of Wnt signaling genes. Feathers from different body regions also showed differential expression of Hox genes. The two subspecies differed in expression of ASIP and three other genes (MFSD12, KCNJ13, HAND2) previously associated with color development. Sequence variation in the expressed genes was not related to color differences between junco subspecies. Our findings suggest that differential expression of a few genes can account for marked differences in plumage color and pattern, a mechanism that can account for the rapid diversification of juncos. Several novel candidate pigmentation genes found in juncos may contribute to the expression of melanic coloration in other vertebrates.