The Evolution of HoxD-11 Expression in the Bird Wing: Insights from Alligator mississippiensis
Publication Date
October 03, 2008
Journal
PLOS ONE
Authors
Alexander O. Vargas, Tiana Kohlsdorf, John F. Fallon, John Vanden Brooks, et al
Volume
3
Issue
10
Pages
e3325
DOI
https://dx.plos.org/10.1371/journal.pone.0003325
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0003325
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/18833328
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2553264
Europe PMC
http://europepmc.org/abstract/MED/18833328
Web of Science
000264797400003
Scopus
53749084655
Mendeley
http://www.mendeley.com/research/evolution-hoxd11-expression-bird-wing-insights-alligator-mississippiensis
Events
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/919688"], "description"=>"<p>A) Embryology: In pentadactyl amniotes like mammals and crocodilians, the primary axis of cartilage formation (red line) always develops into digit 4. Embryological condensations in this figure are labeled C1–C5 based on their spatial relation to the primary axis (C4). B) Gene expression (Late phase): In the mouse, expression of <i>HoxD10-D12</i> is absent only in digit 1. In the chicken, expression is absent in the anterior digit, but it is one position closer to the primary axis, at the embryological position of C2. C) Comparative morphology: The wing digits are morphologically 1, 2, and 3. The hypothesis of a homeotic frame shift proposes that digits 1,2 and 3 have all shifted one embryological position towards posterior in the evolution of the bird line, such that digits D1, D2 and D3 (color coded: cream, blue and green) in the wing develop from the embryological positions C2, C3 and C4. If the frame shift hypothesis is correct, we expect to find that HoxD gene expression in crocodilians will be absent only at embryological position C1.</p>", "links"=>[], "tags"=>["levels", "avian", "digit", "homology"], "article_id"=>590138, "categories"=>["Evolutionary Biology", "Developmental Biology"], "users"=>["Alexander O. Vargas", "Tiana Kohlsdorf", "John F. Fallon", "John VandenBrooks", "Günter P. Wagner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003325.g001", "stats"=>{"downloads"=>2, "page_views"=>40, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_levels_to_the_avian_digit_homology_problem_embryology_gene_expression_and_morphology_/590138", "title"=>"Three levels to the avian digit homology problem: embryology, gene expression, and morphology.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 07:57:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/920010"], "description"=>"<p>A) The expression of <i>HoxD-11</i> in the developing forelimb and hind limb of the crocodilian <i>Alligator mississippiensis</i> (staging is according to Ferguson <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003325#pone.0003325-Wagner3\" target=\"_blank\">[29]</a>) B) The expression of <i>HoxD-11</i> in the chicken <i>Gallus gallus</i> (staging according to Hamburger-Hamilton <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003325#pone.0003325-Ferguson1\" target=\"_blank\">[30]</a>). Alligator forelimb: Early stages 12–14 show extension of <i>HoxD-11</i> along the limb border, including anterior regions (black arrows). At stage 16 and onwards, there is no detectable expression in the anterior-most digit 1 region. At stage 16 posterior expression is temporarily down-regulated in the region of digits 4 and 5 (black arrow) but is re-expressed by stage 17. At stage 17, only very low expression is detectable in the interdigit between digit 1 and 2 (black arrow). Strong anterior and posterior expression in the wrist and forearm region at stage 14 continues up to stage 17 (white arrows). Alligator hind limb: Stage 12 shows some expression along the anterior margin (white arrow) but this is undetectable in the anterior-most digit 1 region from stage 14 onwards. At stage 16, only very low expression is detectable in the interdigit between digits 1 and 2 (black arrow). Expression in the foreleg is restricted to posterior (stages 12 and 14, black arrow) and absent in the ankle region. Stage 17 and stage 18 show a sharp anterior limit of <i>HoxD-11</i> expression along the posterior margin of digit 2 (white arrows). Chicken wing: Stage 24 presents anterior expression (black arrow). Expression is undetectable in digit 1 in stage 26 and subsequent stages. No low expression is detectable between interdigits 1 and 2. In stages 26–34, expression of <i>HoxD-11</i> extends to the anterior border of digit 2 (black arrows). Chicken hind limb: Early stage 24 shows no anterior expression. No expression is ever detected in digit 1 precursor cells or the interdigit between digit 1 and digit 2. In stages 29–34 <i>HoxD-11</i> shows a sharp anterior limit along the posterior border of digit 2 (black arrows in stage 17–18 of alligator and stages 31–34 of chicken; stage 34 is shown in ventral view). Strong expression is found in the interdigit between digits 2 and 3 (stage 29, black arrow), as in forelimbs. <i>HoxD-11</i> expression in alligator limbs is consistent with the notion that, as in chicken, normal digit 1 determination occurs at late stages with absent or very low <i>HoxD-11</i> expression.</p>", "links"=>[], "tags"=>["alligator"], "article_id"=>590462, "categories"=>["Evolutionary Biology", "Developmental Biology"], "users"=>["Alexander O. Vargas", "Tiana Kohlsdorf", "John F. Fallon", "John VandenBrooks", "Günter P. Wagner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003325.g004", "stats"=>{"downloads"=>15, "page_views"=>36, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_expression_of_HoxD_11_in_alligator_and_chicken_limbs_/590462", "title"=>"The expression of <i>HoxD-11</i> in alligator and chicken limbs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 08:00:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/919936"], "description"=>"<p>(EU597806): A) alignment of the deduced alligator amino acid sequence with the <i>HoxD-11</i> sequence of chicken. In exon 1 the amino acid sequence conservation is 87%. B) Maximum parsimony tree of the aligned exon 1 amino acid sequences from <i>HoxD-11</i>, <i>HoxA-11</i> and <i>HoxC-11</i> sequences. C) Neighbor joining tree of the aligned exon 1 amino acid sequences from <i>HoxD-11</i>, <i>HoxA-11</i> and <i>HoxC-11</i> sequences. B+C) The numbers at the internal branches represent bootstrap support values. Note that the alligator <i>HoxD-11</i> sequence, AmiHoxd11, forms a well-supported clade with the human, HsaHoxd11, and the chicken, GgaHoxd11, <i>HoxD-11</i> sequences, confirming that the alligator sequence is a <i>HoxD-11</i> ortholog. Furthermore, the alligator sequence is more closely related to the chicken sequence than to the mouse sequence, as expected based on the accepted species phylogeny. D) Expression of the alligator sequence in a stage 12 alligator embryo. The embryo is dissected to show the sharp anterior limit of hindgut expression (1). Expression is also present in genital tubercule (2), distal tail (3) and limb buds (4), all known expression domains of <i>HoxD-11</i> in chicken and mouse that confirm the alligator sequence is a homolog of <i>HoxD-11</i>.</p>", "links"=>[], "tags"=>["alligator", "exon"], "article_id"=>590389, "categories"=>["Evolutionary Biology", "Developmental Biology"], "users"=>["Alexander O. Vargas", "Tiana Kohlsdorf", "John F. Fallon", "John VandenBrooks", "Günter P. Wagner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003325.g003", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_the_alligator_HoxD_11_exon_1_sequence_/590389", "title"=>"Identification of the alligator <i>HoxD-11</i> exon 1 sequence.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 07:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/919823"], "description"=>"<p>The forelimb and hind limbs of representative taxa illustrate the history of digit morphology in the lineages leading to the taxa compared in this study, the chicken (<i>Gallus gallus</i>), alligator (<i>Alligator mississippiensis</i>) and mouse (<i>Mus musculus</i>). The digits of early birds like <i>Archaeopteryx</i>, are specifically similar to digits 1, 2, and 3 of crocodilians, presenting 2,3 and 4 phalanges on each digit, respectively (node Ar). We arrive at the same conclusion if we compare <i>Archaeopteryx</i> to early dinosaurs, lizards, and early branches of amniotes (such as <i>Captorhinus</i>, <i>Ophiacodon</i>). No comparative morphological evidence has been presented for a 2,3,4 identification of wing digits. Molecular phylogenies confirm the relationships shown in this figure <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003325#pone.0003325-Lee1\" target=\"_blank\">[3]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003325#pone.0003325-Meyer1\" target=\"_blank\">[33]</a>. Maximally parsimonious inference of morphological history is done following the method in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003325#pone.0003325-Donoghue1\" target=\"_blank\">[34]</a>. The nodes of the tree are labeled for corresponding clades: A) Amniota R) Reptilia, D) Diapsida, Ar) Archosauria, T) Theropoda, B) Birds S) Synapsida Th) Therapsida. A geological time scale indicates the approximate time of lineage divergence.</p>", "links"=>[], "tags"=>["digit"], "article_id"=>590278, "categories"=>["Evolutionary Biology", "Developmental Biology"], "users"=>["Alexander O. Vargas", "Tiana Kohlsdorf", "John F. Fallon", "John VandenBrooks", "Günter P. Wagner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003325.g002", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_evolution_of_digit_morphology_/590278", "title"=>"The evolution of digit morphology.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 07:58:48"}

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Relative Metric

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