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Figure1. The Laysan Albatross
(Phoebastria immutabilis)
(https://ebird.org/species/layalb)
The Embryogenesis of the Manus of the Laysan Albatross (Phoebastria immutabilis)
1
1
2
Ryan D. Bastyr , Susan J Rehorek , Timothy D. Smith
1Department Of Biology, SRU, PA, 2Department of Physical Therapy, SRU, PA
Introduction
The basic structure of the avian forelimb consists of 3 digits
supported by corresponding metacarpals, the carpals os carpi
radiale and os carpi ulnare, the radius, and the ulna. (Baumel and
Wittmer, 1993). The conversion of a 5-digit hand to a 3-digit hand
occurred in their dinosaur ancestors and was passed down to
modern birds. (Barta et al., 2017).
Discrepancies in forelimb identity and homology are long
debated topics between dinosaur paleontologists and bird
embryologists. (Burke and Fedducia, 1997). Dinosaur
paleontologist believe the numeration of the digits to be I-II-III
while Bird embryologists believe it to be II-III-IV. (Bothelo et al.
2014: Baumels and Wittmer, 1993). Dinosaur paleontologist
believe the homology of the carpals to be a radiale and an ulnare
while bird embryologists believe it to be a scapholunare and a
pisiform for the os carpi radiale and the os carpi ulnare
respectively. (Bothelo et al. 2014: Baumels and Wittmer, 1993)
The Laysan albatross is a large pelagic bird with a long
incubation period of 65 days (Prum, 2002). The embryos exhibit
transient primitive features in their elongated development which
could help give insight into the evolution and homologies of the
avian hand (Rehorek et al., 2016).
I II III IV V
I II III IV V
Paleontology
Embryology
Figure 2. Simplified pentadactyl hands showing
believed finger conservation from the standpoints
of paleontologists and embryologists. Conserved
fingers are depicted in green while fingers lost in
evolution are depicted in red.
Results and Discussion
Abbreviations: H:Humerus; R:Radius; U:Ulna; RL: Radiale; UL: Ulnare; P:Pisiform; C1:
Embryonic carpal 1; C2: Embryonic carpal 2; C3: Embryonic carpal 3; I/II/III/IV/V: Digits
I/II/III/IV/V respectively
A
Plate 5. A palmar view of the albatross manus at day 28 (stage 37). B depicts an overlay of the
outlines giving a full context to the manus. Complete degeneration of the ulnare leaves the
pisiform as the primary center for ossification on the lateral side of the manus showing that it
will become the os carpi ulnare. Metacarpal V is still present at this stage. Scale Bar = 3mm
A
B
Plate 1. A palmar view of the albatross manus at day 19 (stage 31). B depicts an overlay of the
outlines giving a dorsal view for full context of the manus. The carpals are still in development and a
transient fifth metacarpal (V) is present starting at this stage. Scale Bar = 4mm
Conclusion
•
•
•
A
B
Plate 2. A medial view of the albatross manus at day 21 (stage 32). B depicts an overlay of the
outlines giving a full context to the manus. The maximum number of embryonic carpals are present,
metacarpal V is still visible, and the embryonic ulnare is starting to degenerate. Scale Bar = 5mm
•
•
•
Figure 3. the structure of the forelimb in
birds which correlates with the that of the
Laysan Albatross. (etc.usf.edu)
Materials & Methods
The forelimbs of albatrosses from days 15, 19, 21, 23, 25, and
28 of development (embryonic stages 29, 31, 32, 34, 36, and 37)
were prepared for paraffin histology and serially sectioned at a 10micron thickness. The sections were stained with a Masson’s
trichrome stain and photographed using a Zeiss microscope at 25x
magnification with digital imaging capabilities.
Using Adobe photoshop 2021 the sections for each day were
digitally aligned. Each cartilage condensation, which is a precursor
for bone generation, was outlined and filled in on separate layers
from the original photos. The layers containing the filled in
outlines were then exported as individual tiff format images.
B
A
B
Plate 3. A medial view of the albatross manus at day 23 (stage 34). B depicts an overlay of the
outlines giving a full context to the manus. C1, C2, and C3 are lined up and, C2 and C3 begin to fuse
into a semilunate carpal. Metacarpal V is still present at this stage. Scale Bar = 3mm
•
A study showing that ostriches contain precursors for digits I and
V in early embryogenesis supports the proper identification of
digit V in the Albatross (Feduccia and Nowicki, 2002)
The presence of a transient metacarpal V supports the numbering
of digits as II-III-IV.
Degeneration of the embryonic radiale supports that the os carpi
ulnare is a pisiform, supporting homologies proposed by bird
embryologists and also seen in Bothelo et al. (2014).
Formation of an embryonic semilunate from embryonic carpals 2
& 3 support a Bird-therapod link. (Xu et al., 2014)
Studies involving chicken embryos and immunofluorescent
staining for type II and IX collagen expression showed distinct
foci in the semilunate and radiale suggesting the fusion of
embryonic carpals for formation (Bothelo et al., 2014).
Future investigation using florescent immunohistochemistry in
earlier embryonic stages could help clarify homologies of the
carpals or reveal other possible primitive features.
Future investigations using birds with longer incubation periods,
like the Kiwi (74-84 days) could be used to investigate the
possibility of other primitive features (Reid and Williams, 1975)
References
Barta, D.E., Nesbit S.J., Norell, M.A. 2017. The Evolution of the Manus by Early Therapod Dinosaurs is Characterized by High Inter- and
Intraspecific Variation. Journal of Anatomy. 232(1): 80-104
Baumel J.J, Witmer, L.A. 1993. Osteologia. Nomina Anatomica Avium. (2)45-132
Botelho, J.F., Ossa-fuentes, L., Soto-Acuna, A., Smith-Paredes, D., Nunez-Leon, D., Salinas-Saavedra, M., Ruiz-Flores, Vargas, A.O., 2014. New
Developmental Evidence Clarifies the Evolution of Wrist Bones in the Dinosaur–Bird Transition. PLOS Biology, 12(9):1-13
Burke, A.C. Fedducia, A. 1997. Developmental Patterns and Identification of Homologies in the Avian Hand. Science. 278(5338), 666-668
A
B
Fedducia, A., Nowicki, J. 2002. The hand of birds revealed by early ostrich embryos. Naturwissenschaft. 89:391-393
Prum, R.O. 2002. Why Ornithologist Should Care about the Therapod Origin of Birds. The Auk. 119(1):1-17
Rehorek, S.J., Smith, T.D., Beeching, S.C. 2016. Early Development and Differentiation of the Laysan Albatross (Phoebastria immutabilis).
Plate 4. A palmar view of the albatross manus at day 25 (stage 36). B depicts an overlay of the
outlines giving a full context to the manus. Fusion into a singular carpal proximal to metacarpals
shows that a semilunate carpal had formed before C1 will fuse with the metacarpals of III and IV.
Metacarpal V is still present at this stage. Scale Bar = 1mm
(Rothschild, 1893)): Procellariforms. Journal of Morphology. 277:1231-1249
Reid, B., Williams, G.R. 1975. The Kiwi. Biogeography and Ecology in New Zealand. 1975. 301-330
Vasquez, R.J. 1992. Functional osteology of the avian wrist and the evolution of flapping flight. Journal of morphology. 211(3):259-268
Xu, X., Han F., Zhao, Q. 2014, Homologies and homeotic transformation of the therapod ‘Semilunate’ Carpal. Scientific Reports
(Phoebastria immutabilis)
(https://ebird.org/species/layalb)
The Embryogenesis of the Manus of the Laysan Albatross (Phoebastria immutabilis)
1
1
2
Ryan D. Bastyr , Susan J Rehorek , Timothy D. Smith
1Department Of Biology, SRU, PA, 2Department of Physical Therapy, SRU, PA
Introduction
The basic structure of the avian forelimb consists of 3 digits
supported by corresponding metacarpals, the carpals os carpi
radiale and os carpi ulnare, the radius, and the ulna. (Baumel and
Wittmer, 1993). The conversion of a 5-digit hand to a 3-digit hand
occurred in their dinosaur ancestors and was passed down to
modern birds. (Barta et al., 2017).
Discrepancies in forelimb identity and homology are long
debated topics between dinosaur paleontologists and bird
embryologists. (Burke and Fedducia, 1997). Dinosaur
paleontologist believe the numeration of the digits to be I-II-III
while Bird embryologists believe it to be II-III-IV. (Bothelo et al.
2014: Baumels and Wittmer, 1993). Dinosaur paleontologist
believe the homology of the carpals to be a radiale and an ulnare
while bird embryologists believe it to be a scapholunare and a
pisiform for the os carpi radiale and the os carpi ulnare
respectively. (Bothelo et al. 2014: Baumels and Wittmer, 1993)
The Laysan albatross is a large pelagic bird with a long
incubation period of 65 days (Prum, 2002). The embryos exhibit
transient primitive features in their elongated development which
could help give insight into the evolution and homologies of the
avian hand (Rehorek et al., 2016).
I II III IV V
I II III IV V
Paleontology
Embryology
Figure 2. Simplified pentadactyl hands showing
believed finger conservation from the standpoints
of paleontologists and embryologists. Conserved
fingers are depicted in green while fingers lost in
evolution are depicted in red.
Results and Discussion
Abbreviations: H:Humerus; R:Radius; U:Ulna; RL: Radiale; UL: Ulnare; P:Pisiform; C1:
Embryonic carpal 1; C2: Embryonic carpal 2; C3: Embryonic carpal 3; I/II/III/IV/V: Digits
I/II/III/IV/V respectively
A
Plate 5. A palmar view of the albatross manus at day 28 (stage 37). B depicts an overlay of the
outlines giving a full context to the manus. Complete degeneration of the ulnare leaves the
pisiform as the primary center for ossification on the lateral side of the manus showing that it
will become the os carpi ulnare. Metacarpal V is still present at this stage. Scale Bar = 3mm
A
B
Plate 1. A palmar view of the albatross manus at day 19 (stage 31). B depicts an overlay of the
outlines giving a dorsal view for full context of the manus. The carpals are still in development and a
transient fifth metacarpal (V) is present starting at this stage. Scale Bar = 4mm
Conclusion
•
•
•
A
B
Plate 2. A medial view of the albatross manus at day 21 (stage 32). B depicts an overlay of the
outlines giving a full context to the manus. The maximum number of embryonic carpals are present,
metacarpal V is still visible, and the embryonic ulnare is starting to degenerate. Scale Bar = 5mm
•
•
•
Figure 3. the structure of the forelimb in
birds which correlates with the that of the
Laysan Albatross. (etc.usf.edu)
Materials & Methods
The forelimbs of albatrosses from days 15, 19, 21, 23, 25, and
28 of development (embryonic stages 29, 31, 32, 34, 36, and 37)
were prepared for paraffin histology and serially sectioned at a 10micron thickness. The sections were stained with a Masson’s
trichrome stain and photographed using a Zeiss microscope at 25x
magnification with digital imaging capabilities.
Using Adobe photoshop 2021 the sections for each day were
digitally aligned. Each cartilage condensation, which is a precursor
for bone generation, was outlined and filled in on separate layers
from the original photos. The layers containing the filled in
outlines were then exported as individual tiff format images.
B
A
B
Plate 3. A medial view of the albatross manus at day 23 (stage 34). B depicts an overlay of the
outlines giving a full context to the manus. C1, C2, and C3 are lined up and, C2 and C3 begin to fuse
into a semilunate carpal. Metacarpal V is still present at this stage. Scale Bar = 3mm
•
A study showing that ostriches contain precursors for digits I and
V in early embryogenesis supports the proper identification of
digit V in the Albatross (Feduccia and Nowicki, 2002)
The presence of a transient metacarpal V supports the numbering
of digits as II-III-IV.
Degeneration of the embryonic radiale supports that the os carpi
ulnare is a pisiform, supporting homologies proposed by bird
embryologists and also seen in Bothelo et al. (2014).
Formation of an embryonic semilunate from embryonic carpals 2
& 3 support a Bird-therapod link. (Xu et al., 2014)
Studies involving chicken embryos and immunofluorescent
staining for type II and IX collagen expression showed distinct
foci in the semilunate and radiale suggesting the fusion of
embryonic carpals for formation (Bothelo et al., 2014).
Future investigation using florescent immunohistochemistry in
earlier embryonic stages could help clarify homologies of the
carpals or reveal other possible primitive features.
Future investigations using birds with longer incubation periods,
like the Kiwi (74-84 days) could be used to investigate the
possibility of other primitive features (Reid and Williams, 1975)
References
Barta, D.E., Nesbit S.J., Norell, M.A. 2017. The Evolution of the Manus by Early Therapod Dinosaurs is Characterized by High Inter- and
Intraspecific Variation. Journal of Anatomy. 232(1): 80-104
Baumel J.J, Witmer, L.A. 1993. Osteologia. Nomina Anatomica Avium. (2)45-132
Botelho, J.F., Ossa-fuentes, L., Soto-Acuna, A., Smith-Paredes, D., Nunez-Leon, D., Salinas-Saavedra, M., Ruiz-Flores, Vargas, A.O., 2014. New
Developmental Evidence Clarifies the Evolution of Wrist Bones in the Dinosaur–Bird Transition. PLOS Biology, 12(9):1-13
Burke, A.C. Fedducia, A. 1997. Developmental Patterns and Identification of Homologies in the Avian Hand. Science. 278(5338), 666-668
A
B
Fedducia, A., Nowicki, J. 2002. The hand of birds revealed by early ostrich embryos. Naturwissenschaft. 89:391-393
Prum, R.O. 2002. Why Ornithologist Should Care about the Therapod Origin of Birds. The Auk. 119(1):1-17
Rehorek, S.J., Smith, T.D., Beeching, S.C. 2016. Early Development and Differentiation of the Laysan Albatross (Phoebastria immutabilis).
Plate 4. A palmar view of the albatross manus at day 25 (stage 36). B depicts an overlay of the
outlines giving a full context to the manus. Fusion into a singular carpal proximal to metacarpals
shows that a semilunate carpal had formed before C1 will fuse with the metacarpals of III and IV.
Metacarpal V is still present at this stage. Scale Bar = 1mm
(Rothschild, 1893)): Procellariforms. Journal of Morphology. 277:1231-1249
Reid, B., Williams, G.R. 1975. The Kiwi. Biogeography and Ecology in New Zealand. 1975. 301-330
Vasquez, R.J. 1992. Functional osteology of the avian wrist and the evolution of flapping flight. Journal of morphology. 211(3):259-268
Xu, X., Han F., Zhao, Q. 2014, Homologies and homeotic transformation of the therapod ‘Semilunate’ Carpal. Scientific Reports