Limits...
The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis.

Vargas AO, Kohlsdorf T, Fallon JF, Vandenbrooks J, Wagner GP - PLoS ONE (2008)

Bottom Line: Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos.The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1.HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA. thearchosaur@gmail.com

ABSTRACT

Background: Comparative morphology identifies the digits of the wing of birds as 1,2 and 3, but they develop at embryological positions that become digits 2, 3 and 4 in other amniotes. A hypothesis to explain this is that a homeotic frame shift of digital identity occurred in the evolution of the bird wing, such that digits 1,2 and 3 are developing from embryological positions 2, 3 and 4. Digit 1 of the mouse is the only digit that shows no late expression of HoxD-11. This is also true for the anterior digit of the bird wing, suggesting this digit is actually a digit 1. If this is the case, we can expect closer relatives of birds to show no HoxD-11 expression only in digit 1. To test this prediction we investigate HoxD-11 expression in crocodilians, the closest living relatives of birds.

Methodology/principal findings: Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos. We found that in the pentadactyl forelimbs of alligator, as in the mouse, late expression of HoxD-11 is absent only in digit 1.

Conclusions/significance: The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1. The biphalangeal morphology and lack of HoxD-11 expression of the anterior digit of the wing is like digit 1 of alligator and mouse, but its embryological position as digit 2 is derived. HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing.

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Three levels to the avian digit homology problem: embryology, gene expression, and morphology.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 HoxD10-D12 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.
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pone-0003325-g001: Three levels to the avian digit homology problem: embryology, gene expression, and morphology.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 HoxD10-D12 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.

Mentions: The identity of the digits of the bird wing is a classic problem of evolutionary biology, born out of apparently contradictory developmental and morphological evidence. If we follow the criterion of homology by embryological position of origin, we find that the wing digits develop from embryological positions corresponding to those of digits 2, 3 and 4 of crocodilians [1], [2]. Crocodilians are bird's closest living relatives [3] and thus the optimal reference point for developmental comparisons to the bird wing. In the alligator forelimb (as in mouse) the first cartilaginous digital condensation to form is spatially in line with the ulnare and ulna (Figure 1A, top row), and develops into digit 4 (Figure 1 A, bottom row). The spatial alignment of these elements is referred to as the “primary axis”, indicated by a red line in Figure 1. In the wing, the primary axis develops into the posterior digit, indicating the digits develop at positions 2, 3 and 4 [1], [2] (Figure 1A). However, the wing digits of early birds like Archaeopteryx are morphologically similar to digits 1, 2, and 3 of crocodilians, presenting 2, 3 and 4 phalanges, respectively (Figure 2). We arrive at the same conclusion if we compare Archaeopteryx to early dinosaurs, lizards, and even early branches of amniotes (Figure 2, See Captorhinus, Ophiacodon). Wing digits are labeled 1,2,3 in the fields of phylogenetic systematics and comparative anatomy [4], [5], [6], [7] As an explanation to this apparent contradiction with the embryological evidence, Wagner and Gauthier [8] suggested that a homeotic frame shift of digital identity had occurred in the evolution of the bird wing, such that in birds digits 1, 2 and 3 develop from embryological positions 2, 3 and 4 (Figure 1C).


The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis.

Vargas AO, Kohlsdorf T, Fallon JF, Vandenbrooks J, Wagner GP - PLoS ONE (2008)

Three levels to the avian digit homology problem: embryology, gene expression, and morphology.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 HoxD10-D12 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.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2553264&req=5

pone-0003325-g001: Three levels to the avian digit homology problem: embryology, gene expression, and morphology.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 HoxD10-D12 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.
Mentions: The identity of the digits of the bird wing is a classic problem of evolutionary biology, born out of apparently contradictory developmental and morphological evidence. If we follow the criterion of homology by embryological position of origin, we find that the wing digits develop from embryological positions corresponding to those of digits 2, 3 and 4 of crocodilians [1], [2]. Crocodilians are bird's closest living relatives [3] and thus the optimal reference point for developmental comparisons to the bird wing. In the alligator forelimb (as in mouse) the first cartilaginous digital condensation to form is spatially in line with the ulnare and ulna (Figure 1A, top row), and develops into digit 4 (Figure 1 A, bottom row). The spatial alignment of these elements is referred to as the “primary axis”, indicated by a red line in Figure 1. In the wing, the primary axis develops into the posterior digit, indicating the digits develop at positions 2, 3 and 4 [1], [2] (Figure 1A). However, the wing digits of early birds like Archaeopteryx are morphologically similar to digits 1, 2, and 3 of crocodilians, presenting 2, 3 and 4 phalanges, respectively (Figure 2). We arrive at the same conclusion if we compare Archaeopteryx to early dinosaurs, lizards, and even early branches of amniotes (Figure 2, See Captorhinus, Ophiacodon). Wing digits are labeled 1,2,3 in the fields of phylogenetic systematics and comparative anatomy [4], [5], [6], [7] As an explanation to this apparent contradiction with the embryological evidence, Wagner and Gauthier [8] suggested that a homeotic frame shift of digital identity had occurred in the evolution of the bird wing, such that in birds digits 1, 2 and 3 develop from embryological positions 2, 3 and 4 (Figure 1C).

Bottom Line: Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos.The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1.HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA. thearchosaur@gmail.com

ABSTRACT

Background: Comparative morphology identifies the digits of the wing of birds as 1,2 and 3, but they develop at embryological positions that become digits 2, 3 and 4 in other amniotes. A hypothesis to explain this is that a homeotic frame shift of digital identity occurred in the evolution of the bird wing, such that digits 1,2 and 3 are developing from embryological positions 2, 3 and 4. Digit 1 of the mouse is the only digit that shows no late expression of HoxD-11. This is also true for the anterior digit of the bird wing, suggesting this digit is actually a digit 1. If this is the case, we can expect closer relatives of birds to show no HoxD-11 expression only in digit 1. To test this prediction we investigate HoxD-11 expression in crocodilians, the closest living relatives of birds.

Methodology/principal findings: Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos. We found that in the pentadactyl forelimbs of alligator, as in the mouse, late expression of HoxD-11 is absent only in digit 1.

Conclusions/significance: The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1. The biphalangeal morphology and lack of HoxD-11 expression of the anterior digit of the wing is like digit 1 of alligator and mouse, but its embryological position as digit 2 is derived. HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing.

Show MeSH
Related in: MedlinePlus