Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Comparative Study
. 2015 Jan;32(1):23-8.
doi: 10.1093/molbev/msu309. Epub 2014 Nov 18.

Feather Development Genes and Associated Regulatory Innovation Predate the Origin of Dinosauria

Affiliations
Free PMC article
Comparative Study

Feather Development Genes and Associated Regulatory Innovation Predate the Origin of Dinosauria

Craig B Lowe et al. Mol Biol Evol. .
Free PMC article

Abstract

The evolution of avian feathers has recently been illuminated by fossils and the identification of genes involved in feather patterning and morphogenesis. However, molecular studies have focused mainly on protein-coding genes. Using comparative genomics and more than 600,000 conserved regulatory elements, we show that patterns of genome evolution in the vicinity of feather genes are consistent with a major role for regulatory innovation in the evolution of feathers. Rates of innovation at feather regulatory elements exhibit an extended period of innovation with peaks in the ancestors of amniotes and archosaurs. We estimate that 86% of such regulatory elements and 100% of the nonkeratin feather gene set were present prior to the origin of Dinosauria. On the branch leading to modern birds, we detect a strong signal of regulatory innovation near insulin-like growth factor binding protein (IGFBP) 2 and IGFBP5, which have roles in body size reduction, and may represent a genomic signature for the miniaturization of dinosaurian body size preceding the origin of flight.

Keywords: body size; comparative genomics; dinosaur; enhancer; gene regulation; integument.

Figures

F<sc>ig</sc>. 1.
Fig. 1.
Feather development genes are ancient whereas associated CNEEs peak in the amniote ancestor. Evolutionary dynamics of (a) nonkeratin feather development genes and associated CNEEs (n = 126 genes) and (b) keratin genes and associated CNEEs (n = 67 genes). The black horizontal line indicates the null expectation of the number of new genes (comparison to all genes in the genome) or CNEEs (a uniform distribution throughout the genome). Points above this line indicate lineages on which a higher-than-expected number of genes or CNEEs have arisen. Points on the x axis correspond to the ancestors depicted in figure 2, with spacing proportional to divergence times as recorded in timetree.org (Hedges et al. 2006). In (b), the larger peak comprised β-keratins arising from expansions of gene clusters on chicken chromosomes 27 and 2. The small peak in the turtle-bird ancestor is due to the expansion of a β-keratin gene cluster on chromosome 25. Both of these results are consistent with previous studies of β-keratin evolution (Greenwold and Sawyer 2010; Li et al. 2013).
F<sc>ig</sc>. 2.
Fig. 2.
Major genomic events underlying the origin of feathers. The colored backbone of the tree shows three tracks: CNEEs, nonkeratin feather genes (n = 126), and keratin genes (n = 67). Rates of origination of these three genomic classes are indicated by the colors for each stem internode and track in the tree, with blue colors indicating low origination rates and red colors indicating high origination rates. Key events at the level of coding regions (genes) and regulatory elements are indicated. The colors of the silhouettes at right indicate the percent of the feather regulatory component present in the chicken genome inferred to have arisen in the ancestor of each indicated taxon. For example, the fish are inferred to possess about 28% of the CNEEs associated with feather genes in chicken, whereas 86% of the observed chicken CNEEs are inferred to have arisen by the ancestral archosaur, including nonavian dinosaurs.
F<sc>ig</sc>. 3.
Fig. 3.
Identification of regions of the avian genome with signatures of exceptional regulatory innovation on the archosaur lineage that includes birds and other dinosaurs. (a) A genome-wide plot of the density of CNEEs arising on the archosaurian branch leading to the avian ancestor. Red regions indicate those areas enriched compared with the distribution of CNEEs on other branches (gray line in [b]) and green squares indicate the 23 significant peaks of enrichment for bird-specific CNEEs relative to a uniform distribution throughout the genome. We examined the closest upstream and closest downstream genes and for select peaks a flanking gene is indicated along with a proposed role in avian morphological evolution (key at top); regulatory innovation may also have played a role in earlier dinosaur-lineage evolutionary dynamics. (b) The densest region for bird-specific CNEEs in the chicken genome is in a gene desert on chromosome 7 with IGFBP2 being the closest well-annotated refseq gene and IGFBP5 being the closest gene prediction. CNEE density on all branches other than the one leading to birds is indicated in gray. (c) UCSC Genome Browser shot of a CNEE-rich region in the vicinity of IGFBP2 and IGFBP5, which functions in limb development and body size regulation (see main text, supplementary table S4, Supplementary Material online), showing CNEEs found only in birds (red boxes) or arising on deeper branches in the vertebrate tree (gray boxes). Regions of aligning sequence for representatives of the 19 included taxa are in green.

Similar articles

See all similar articles

Cited by 21 articles

See all "Cited by" articles

References

    1. Alibardi L. Perspectives on hair evolution based on some comparative studies on vertebrate cornification. J Exp Zool B Mol Dev Evol. 2012;318:325–343. - PubMed
    1. Alibardi L, Dalla Valle L, Nardi A, Toni M. Evolution of hard proteins in the sauropsid integument in relation to the cornification of skin derivatives in amniotes. J Anat. 2009;214:560–586. - PMC - PubMed
    1. Antin PB, Yatskievych TA, Davey S, Darnell DK. GEISHA: an evolving gene expression resource for the chicken embryo. Nucleic Acids Res. 2014;42:D933–D937. - PMC - PubMed
    1. Benson RBJ, Campione NE, Carrano MT, Mannion PD, Sullivan C, Upchurch P, Evans DC. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biol. 2014;12:e1001853. doi:10.1371/journal.pbio.1001853. - PMC - PubMed
    1. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science. 2010;327:302–305. - PMC - PubMed

Publication types

Substances

Feedback