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Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species

Published on Mar 15, 2016in eLife7.55
· DOI :10.7554/eLife.12115
Eric T. Domyan7
Estimated H-index: 7
(UofU: University of Utah),
Zev N. Kronenberg14
Estimated H-index: 14
(UofU: University of Utah)
+ 11 AuthorsMichael D. Shapiro31
Estimated H-index: 31
(UofU: University of Utah)
Cite
Abstract
Birds display remarkable diversity in the distribution and morphology of scales and feathers on their feet, yet the genetic and developmental mechanisms governing this diversity remain unknown. Domestic pigeons have striking variation in foot feathering within a single species, providing a tractable model to investigate the molecular basis of skin appendage differences. We found that feathered feet in pigeons result from a partial transformation from hindlimb to forelimb identity mediated by cis-regulatory changes in the genes encoding the hindlimb-specific transcription factor Pitx1 and forelimb-specific transcription factor Tbx5. We also found that ectopic expression of Tbx5 is associated with foot feathers in chickens, suggesting similar molecular pathways underlie phenotypic convergence between these two species. These results show how changes in expression of regional patterning genes can generate localized changes in organ fate and morphology, and provide viable molecular mechanisms for diversity in hindlimb scale and feather distribution.
  • References (73)
  • Citations (25)
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References73
Newest
Published on Dec 1, 2015in Science Advances
Santiago Claramunt11
Estimated H-index: 11
(AMNH: American Museum of Natural History),
Joel Cracraft42
Estimated H-index: 42
(AMNH: American Museum of Natural History)
Determining the timing of diversification of modern birds has been difficult. We combined DNA sequences of clock-like genes for most avian families with 130 fossil birds to generate a new time tree for Neornithes and investigated their biogeographic and diversification dynamics. We found that the most recent common ancestor of modern birds inhabited South America around 95 million years ago, but it was not until the Cretaceous-Paleogene transition (66 million years ago) that Neornithes began to ...
Published on Dec 1, 2015in BMC Evolutionary Biology3.04
Tobin L. Hieronymus9
Estimated H-index: 9
(NEOMED: Northeast Ohio Medical University)
Background Among living fliers (birds, bats, and insects), birds display relatively high aspect ratios, a dimensionless shape variable that distinguishes long and narrow vs. short and broad wings. Increasing aspect ratio results in a functional tradeoff between low induced drag (efficient cruise) and increased wing inertia (difficult takeoff). Given the wide scope of its functional effects, the pattern of aspect ratio evolution is an important factor that contributes to the substantial ecologica...
Published on Oct 1, 2015in Molecular Biology and Evolution14.80
Anna I. Vickrey5
Estimated H-index: 5
(UofU: University of Utah),
Eric T. Domyan7
Estimated H-index: 7
(UofU: University of Utah)
+ 1 AuthorsMichael D. Shapiro31
Estimated H-index: 31
(UofU: University of Utah)
Head crests are important display structures in wild bird sp ecies and are also common in domesticated lineages. Many breeds of domestic rock pigeon (Columba livia) have crests of reversed occipital feathers, and this recessive trait is associated with a nonsynonymous coding mutation in the intracellular kinase domain of EphB2 (Ephrin receptor B2). The domestic ringneck dove (Streptopelia risoria) also has a recessive crested morph with reversed occipital feathers, and interspecific crosses betw...
Published on Jul 25, 2014in Science41.04
Pascal Godefroit20
Estimated H-index: 20
(Royal Belgian Institute of Natural Sciences),
Sofia M. Sinitsa2
Estimated H-index: 2
+ 5 AuthorsPaul Spagna7
Estimated H-index: 7
(Royal Belgian Institute of Natural Sciences)
Middle Jurassic to Early Cretaceous deposits from northeastern China have yielded varied theropod dinosaurs bearing feathers. Filamentous integumentary structures have also been described in ornithischian dinosaurs, but whether these filaments can be regarded as part of the evolutionary lineage toward feathers remains controversial. Here we describe a new basal neornithischian dinosaur from the Jurassic of Siberia with small scales around the distal hindlimb, larger imbricated scales around the ...
Published on Jul 1, 2014in Nature43.07
Christian Foth11
Estimated H-index: 11
,
Helmut Tischlinger3
Estimated H-index: 3
,
Oliver W. M. Rauhut28
Estimated H-index: 28
The discovery of numerous feathered dinosaurs and early birds has set the iconic 'Urvogel' (or 'first bird') Archaeopteryx in a broader context. But this venerable taxon still has the capacity to surprise. A newly discovered specimen from the Solnhofen limestone in Bavaria only the eleventh since 1861 shows a generous covering of feathers all over the body. Of particular note is a hindlimb covering resembling feathered 'trousers'. Analysis of feather distribution on the limbs and tail strongly s...
Published on Feb 1, 2014in Current Biology9.19
Eric T. Domyan7
Estimated H-index: 7
(UofU: University of Utah),
Michael W. Guernsey5
Estimated H-index: 5
(UofU: University of Utah)
+ 9 AuthorsJohn W. Fondon6
Estimated H-index: 6
(UTA: University of Texas at Arlington)
Summary Understanding the molecular basis of phenotypic diversity is a critical challenge in biology, yet we know little about the mechanistic effects of different mutations and epistatic relationships among loci that contribute to complex traits. Pigmentation genetics offers a powerful model for identifying mutations underlying diversity and for determining how additional complexity emerges from interactions among loci. Centuries of artificial selection in domestic rock pigeons ( Columba livia ...
Published on Oct 1, 2013in G3: Genes, Genomes, Genetics2.63
Takahito Shikano19
Estimated H-index: 19
(UH: University of Helsinki),
Veronika N. Laine10
Estimated H-index: 10
(UTU: University of Turku)
+ 2 AuthorsJuha Merilä68
Estimated H-index: 68
(UH: University of Helsinki)
Teleost fish genomes are known to be evolving faster than those of other vertebrate taxa. Thus, fish are suited to address the extent to which the same vs. different genes are responsible for similar phenotypic changes in rapidly evolving genomes of evolutionary independent lineages. To gain insights into the genetic basis and evolutionary processes behind parallel phenotypic changes within and between species, we identified the genomic regions involved in pelvic reduction in Northern European n...
Published on Mar 15, 2013in Science41.04
Xiaoting Zheng15
Estimated H-index: 15
(LYU: Linyi University),
Zhonghe(周忠和) Zhou1
Estimated H-index: 1
(CAS: Chinese Academy of Sciences)
+ 6 AuthorsXing(徐星) Xu1
Estimated H-index: 1
(LYU: Linyi University)
Recent discoveries of large leg feathers in some theropods have implications for our understanding of the evolution of integumentary features on the avialan leg, and particularly of their relevance for the origin of avialan flight. Here we report 11 basal avialan specimens that will greatly improve our knowledge of leg integumentary features among early birds. In particular, they provide solid evidence for the existence of enlarged leg feathers on a variety of basal birds, suggest that extensive...
Published on Mar 1, 2013in Briefings in Bioinformatics9.10
Helga Thorvaldsdottir12
Estimated H-index: 12
,
James Robinson91
Estimated H-index: 91
,
Jill P. Mesirov71
Estimated H-index: 71
Data visualization is an essential component of genomic data analysis. However, the size and diversity of the data sets produced by today’s sequencing and array-based profiling methods present major challenges to visualization tools. The Integrative Genomics Viewer (IGV) is a high-performance viewer that efficiently handles large heterogeneous data sets, while providing a smooth and intuitive user experience at all levels of genome resolution. A key characteristic of IGV is its focus on the inte...
Published on Mar 1, 2013in Science41.04
Michael D. Shapiro31
Estimated H-index: 31
(UofU: University of Utah),
Zev N. Kronenberg14
Estimated H-index: 14
(UofU: University of Utah)
+ 15 AuthorsAnna I. Vickrey5
Estimated H-index: 5
(UofU: University of Utah)
The geographic origins of breeds and the genetic basis of variation within the widely distributed and phenotypically diverse domestic rock pigeon ( Columba livia ) remain largely unknown. We generated a rock pigeon reference genome and additional genome sequences representing domestic and feral populations. We found evidence for the origins of major breed groups in the Middle East and contributions from a racing breed to North American feral populations. We identified the gene EphB2 as a strong ...
Cited By25
Newest
Published on 2019in Avian Biology Research0.85
Mauricio Peñuela1
Estimated H-index: 1
(University of Valle),
Fernando Rondón (Grupo México)+ 1 AuthorsHeiber Cárdenas4
Estimated H-index: 4
(University of Valle)
Published on 2019in Developmental Biology2.94
Elena F. Boer4
Estimated H-index: 4
(UofU: University of Utah),
Hannah F. Van Hollebeke1
Estimated H-index: 1
(UofU: University of Utah)
+ 3 AuthorsMichael D. Shapiro31
Estimated H-index: 31
(UofU: University of Utah)
Abstract The tetrapod limb is a stunning example of evolutionary diversity, with dramatic variation not only among distantly related species, but also between the serially homologous forelimbs (FLs) and hindlimbs (HLs) within species. Despite this variation, highly conserved genetic and developmental programs underlie limb development and identity in all tetrapods, raising the question of how limb diversification is generated from a conserved toolkit. In some breeds of domestic pigeon, shifts in...
Published on Sep 13, 2019in Developmental Dynamics2.85
Daniel Núñez-León1
Estimated H-index: 1
(UZH: University of Zurich),
Gabriel Aguirre-Fernández6
Estimated H-index: 6
(UZH: University of Zurich)
+ 5 AuthorsMarcelo R. Sánchez-Villagra32
Estimated H-index: 32
(UZH: University of Zurich)
Published on 2019in Science41.04
Nina Overgaard Therkildsen14
Estimated H-index: 14
(Cornell University),
Aryn P. Wilder1
Estimated H-index: 1
(Cornell University)
+ 3 AuthorsStephen R. Palumbi79
Estimated H-index: 79
(Stanford University)
Humans cause widespread evolutionary change in nature, but we still know little about the genomic basis of rapid adaptation in the Anthropocene. We tracked genomic changes across all protein-coding genes in experimental fish populations that evolved pronounced shifts in growth rates due to size-selective harvest over only four generations. Comparisons of replicate lines show parallel allele frequency shifts that recapitulate responses to size-selection gradients in the wild across hundreds of un...
Published on Jul 11, 2019in bioRxiv
Lara Busby (University of Sheffield), Christina Aceituno (UC: University of Cantabria)+ 3 AuthorsMatthew Towers10
Estimated H-index: 10
(University of Sheffield)
Flight is a triumph of evolution that enabled the radiation and success of birds. A crucial step was the development of forelimb flight feathers that may have evolved for courtship or territorial displays in ancestral theropod dinosaurs. Classical tissue recombination experiments performed in the chick embryo provide evidence that signals operating during early limb development specify the position and identity of feathers. Here we show that a positional information gradient of Sonic hedgehog (S...
Published on Jul 1, 2019in bioRxiv
Rebecca Bruders (University of Utah Hospital), Hannah F. Van Hollebeke1
Estimated H-index: 1
(UofU: University of Utah)
+ 3 AuthorsMichael D. Shapiro31
Estimated H-index: 31
(UofU: University of Utah)
Rock pigeons (Columba livia) display an extraordinary array of pigment pattern variation. One such pattern, Almond, is characterized by a variegated patchwork of plumage colors that are distributed in an apparently random manner. Almond is a sex-linked, semi-dominant trait controlled by the classical Stipper (St) locus. Heterozygous males (ZStZ+ sex chromosomes) and hemizygous Almond females (ZStW) are favored by breeders for their attractive plumage. In contrast, homozygous Almond males (ZStZSt...
Published on Jan 1, 2019
Elizabeth M. Sefton1
Estimated H-index: 1
(UofU: University of Utah),
Gabrielle Kardon17
Estimated H-index: 17
(UofU: University of Utah)
Abstract Skeletal muscle powers all movement of the vertebrate body and is distributed in multiple regions that have evolved distinct functions. Axial muscles are ancestral muscles essential for support and locomotion of the whole body. The evolution of the head was accompanied by development of cranial muscles essential for eye movement, feeding, vocalization, and facial expression. With the evolution of paired fins and limbs and their associated muscles, vertebrates gained increased locomotor ...
Published on Dec 1, 2018in BMC Ecology2.38
Gavin C. Woodruff3
Estimated H-index: 3
(UO: University of Oregon),
Patrick C. Phillips39
Estimated H-index: 39
(UO: University of Oregon)
Background Biotic interactions are ubiquitous and require information from ecology, evolutionary biology, and functional genetics in order to be understood. However, study systems that are amenable to investigations across such disparate fields are rare. Figs and fig wasps are a classic system for ecology and evolutionary biology with poor functional genetics; Caenorhabditis elegans is a classic system for functional genetics with poor ecology. In order to help bridge these disciplines, here we ...
Published on Dec 1, 2018
Mao Kondo1
Estimated H-index: 1
(Tohoku University),
Tomoe Sekine (Tohoku University)+ 5 AuthorsKoji Tamura34
Estimated H-index: 34
(Tohoku University)
Flight feathers, a type of feather that is unique to extant/extinct birds and some non-avian dinosaurs, are the most evolutionally advanced type of feather. In general, feather types are formed in the second or later generation of feathers at the first and following molting, and the first molting begins at around two weeks post hatching in chicken. However, it has been stated in some previous reports that the first molting from the natal down feathers to the flight feathers is much earlier than ...
Published on Dec 1, 2018in BMC Genomics3.50
Yung-Chih Lai4
Estimated H-index: 4
(SC: University of Southern California),
Ya-Chen Liang1
Estimated H-index: 1
(SC: University of Southern California)
+ 3 AuthorsCheng-Ming Chuong61
Estimated H-index: 61
Background The molecular mechanism controlling regional specific skin appendage phenotypes is a fundamental question that remains unresolved. We recently identified feather and scale primordium associated genes and with functional studies, proposed five major modules are involved in scale-to-feather conversion and their integration is essential to form today’s feathers. Yet, how the molecular networks are wired and integrated at the genomic level is still unknown.
View next paperAdaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer