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Reorganization of mammalian body wall patterning with cloacal septation

Authors:
Margaret I Hall at Midwestern University
Margaret I Hall
Jose Rafael Rodriguez-Sosa at Midwestern University
Jose Rafael Rodriguez-Sosa
Jeffrey H Plochocki at University of Central Florida
Jeffrey H Plochocki
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Abstract and Figures

Septation of the cloaca is a unique mammalian adaptation that required a novel reorganization of the perineum-The caudal portion of the trunk body wall not associated with the hindlimb. Fish, the basal vertebrates, separate ventrolateral body wall musculature of the trunk into two discrete layers, while most tetrapods expand this pattern in the thorax and abdomen into four. Mammals, the only vertebrate group to divide the cloaca into urogenital and anorectal portions, exhibit complex muscle morphology in the perineum. Here we describe how perineal morphology in a broad sample of mammals fits into patterning of trunk musculature as an extension of the four-layer ventrolateral muscular patterning of the thorax and abdomen. We show that each perineal muscle layer has a specific function related to structures formed by cloacal septation. From superficial to deep, there is the subcutaneous layer, which regulates orifice closure, the external layer, which supplements both erectile and micturition function, the internal layer, which provides primary micturition and defecation regulation, and the transversus layer, which provides structural support for pelvic organs. We elucidate how the four-layer body wall pattern, restricted to the non-mammal tetrapod thorax and abdomen, is observed in the mammalian perineum to regulate function of unique perineal structures derived from cloacal septation.
Cladogram of major vertebrate classes demonstrating the evolution of ventrolateral body wall muscle layers. Primitively, vertebrates have two ventrolateral muscle layers, while most tetrapods have four layers in the thorax and abdomen. Mammals exhibit four layers throughout the trunk, including the perineal portion of the body wall.
Cladogram of major vertebrate classes demonstrating the evolution of ventrolateral body wall muscle layers. Primitively, vertebrates have two ventrolateral muscle layers, while most tetrapods have four layers in the thorax and abdomen. Mammals exhibit four layers throughout the trunk, including the perineal portion of the body wall.
… 
Muscles of the ventrolateral body wall in the vertebrate abdomen derived from the embryonic hypaxial and epaxial masses. (A) In fishes, such as teleosts, hypaxial muscles of the ventrolateral wall are organized into two layers (M. obliquus superioris and M. obliquus inferioris). (B) Amphibians, such as salamanders, have two to four layers (M. obliquus externus, in some species divided into superficialis and profundus portions, M. obliquus internus, and M. transversus abdominis, with scattered subcutaneous skeletal muscle fibers). (C) Mammals, like dogs, consistently have four layers (M. cutaneous trunci, a well-developed subcutaneous muscle layer, M. obliquus externus abdominis, M. obliquus internus abdominis and M. transversus abdominis). Development of the ventral musculature, such as M. rectus abdominis, is regulated by different molecular signals and therefore follows a different organizational pattern and may not differentiate into multiple layers 12 .
Muscles of the ventrolateral body wall in the vertebrate abdomen derived from the embryonic hypaxial and epaxial masses. (A) In fishes, such as teleosts, hypaxial muscles of the ventrolateral wall are organized into two layers (M. obliquus superioris and M. obliquus inferioris). (B) Amphibians, such as salamanders, have two to four layers (M. obliquus externus, in some species divided into superficialis and profundus portions, M. obliquus internus, and M. transversus abdominis, with scattered subcutaneous skeletal muscle fibers). (C) Mammals, like dogs, consistently have four layers (M. cutaneous trunci, a well-developed subcutaneous muscle layer, M. obliquus externus abdominis, M. obliquus internus abdominis and M. transversus abdominis). Development of the ventral musculature, such as M. rectus abdominis, is regulated by different molecular signals and therefore follows a different organizational pattern and may not differentiate into multiple layers 12 .
… 
Anatomical organization of the perineal portion of the mammalian trunk body wall into four layers, drawn here after our human dissections. The subcutaneous layer is formed by M. sphincter ani externus pars subcutanea. The external layer includes M. bulbospongiosus, M. ischiocavernosus and M. transversus perinei superficialis. The internal muscle layer is formed by M. sphincter ani externus pars profundus, M. transversus perinei profundus, and the urethral sphincter muscles. The transversus layer includes M. levator ani and M. coccygeus.
Anatomical organization of the perineal portion of the mammalian trunk body wall into four layers, drawn here after our human dissections. The subcutaneous layer is formed by M. sphincter ani externus pars subcutanea. The external layer includes M. bulbospongiosus, M. ischiocavernosus and M. transversus perinei superficialis. The internal muscle layer is formed by M. sphincter ani externus pars profundus, M. transversus perinei profundus, and the urethral sphincter muscles. The transversus layer includes M. levator ani and M. coccygeus.
… 
Perineum of an adult dog in (A) gross dissection (left lateral view, scale bar 5 mm) and (B) histological section (left lateral view, scale bar 5 mm). Histological sections of a fetal bovine aged 15 weeks of the (C) ventrolateral abdominal wall (left anterior view, scale bar 50 µm) and (D) perineum (left lateral view, scale bar 2 mm). Structures labeled 1–4 are 1, subcutaneous layer; 2, external layer; 3, internal layer; and 4, transversus layer. Perineal muscle fibers (B and D) of the subcutaneous layer (1) are shown in crosssection, fiber orientation in the internal and external layers (2 and 3) is oblique, and fiber orientation in the transversus layer (4) is longitudinal in the taxa that have an anus that is shifted to protrude posteriorly, such as the bovine, dog, and horse, but is transverse in other taxa. The fetal muscle layers (D) are closely associated with smooth muscle of the internal anal sphincter and rectum (*) and developing sacral vertebrae (◊). a, artifact; i, integument; SCV, M. sacrocaudalis ventralis, a muscle that acts on the tail.
Perineum of an adult dog in (A) gross dissection (left lateral view, scale bar 5 mm) and (B) histological section (left lateral view, scale bar 5 mm). Histological sections of a fetal bovine aged 15 weeks of the (C) ventrolateral abdominal wall (left anterior view, scale bar 50 µm) and (D) perineum (left lateral view, scale bar 2 mm). Structures labeled 1–4 are 1, subcutaneous layer; 2, external layer; 3, internal layer; and 4, transversus layer. Perineal muscle fibers (B and D) of the subcutaneous layer (1) are shown in crosssection, fiber orientation in the internal and external layers (2 and 3) is oblique, and fiber orientation in the transversus layer (4) is longitudinal in the taxa that have an anus that is shifted to protrude posteriorly, such as the bovine, dog, and horse, but is transverse in other taxa. The fetal muscle layers (D) are closely associated with smooth muscle of the internal anal sphincter and rectum (*) and developing sacral vertebrae (◊). a, artifact; i, integument; SCV, M. sacrocaudalis ventralis, a muscle that acts on the tail.
… 
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
www.nature.com/scientificreports
Reorganization of mammalian
body wall patterning with cloacal
septation
Margaret I. Hall1,2, José R. Rodriguez-Sosa1,2 & Jerey H. Plochocki1
Septation of the cloaca is a unique mammalian adaptation that required a novel reorganization of the
perineum–the caudal portion of the trunk body wall not associated with the hindlimb. Fish, the basal
vertebrates, separate ventrolateral body wall musculature of the trunk into two discrete layers, while
most tetrapods expand this pattern in the thorax and abdomen into four. Mammals, the only vertebrate
group to divide the cloaca into urogenital and anorectal portions, exhibit complex muscle morphology
in the perineum. Here we describe how perineal morphology in a broad sample of mammals ts into
patterning of trunk musculature as an extension of the four-layer ventrolateral muscular patterning
of the thorax and abdomen. We show that each perineal muscle layer has a specic function related to
structures formed by cloacal septation. From supercial to deep, there is the subcutaneous layer, which
regulates orice closure, the external layer, which supplements both erectile and micturition function,
the internal layer, which provides primary micturition and defecation regulation, and the transversus
layer, which provides structural support for pelvic organs. We elucidate how the four-layer body wall
pattern, restricted to the non-mammal tetrapod thorax and abdomen, is observed in the mammalian
perineum to regulate function of unique perineal structures derived from cloacal septation.
Homologous body wall layers that support the vertebrate trunk follow generalized plans that are evolutionarily
conserved and broadly shared among related taxa1, 2. Basal vertebrates, such as teleost shes, have ventrolateral
wall musculature dierentiated into two layers (Figs1 and 2) that function to laterally ex the trunk during
undulatory swimming3. With the transition from water to land, morphological complexity of tetrapod ventro-
lateral body wall musculature in the thorax and abdomen increased as muscle function shied to include trunk
stabilization against torsion and movements of the limbs during terrestrial locomotion4–6. Some basal tetrapods,
such as certain salamanders and frogs, retain two layers throughout the trunk, while other amphibians developed
as many as four layers in the thorax and abdomen7, 8. With the rise of amniotes, which include lizards, crocodiles,
birds, and mammals, the ventrolateral body wall evolved to consistently maintain four layers in the thorax and
abdomen9–12.
Most tetrapods retain the original two vertebrate muscle layers present in shes to regulate opening of the
cloacal orice13, 14. Muscular patterning of the pelvic body wall in mammals, which completely separate the cloaca
to form the anatomical region of the trunk known as the perineum, has yet to be discussed within an evolutionary
context15–17. Perineal muscles in mammals develop between the hindlimb bud and tail, receive innervation from
spinal levels caudal to the hindlimb, attach to axial and pelvic skeletal elements, and support erectile, defecatory,
and micturatory functions of the perineum18. Using a comparative approach, we investigate muscle patterning
in the perineal portion of the mammalian trunk body wall to gain insight into how muscular reconguration
in the perineum compares to the primitive vertebrate body plan. We suggest the muscular pattern for the body
wall present in the tetrapod thorax and abdomen is utilized again in mammals to regulate function of structures
derived from cloacal septation.
Results and Discussion
Our dissections reveal that mammals dierentiate pelvic body wall muscles into four layers, mirroring the tet-
rapod thoracic and abdominal body wall (Figs2 and 3). ese layers include a subcutaneous, external, internal,
1Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, Glendale, AZ, 85308,
USA. 2Department of Anatomy, College of Veterinary Medicine, Midwestern University, Glendale, AZ, 85308, USA.
Margaret I. Hall and Jerey H. Plochocki jointly supervised this work. Correspondence and requests for materials
should be addressed to J.H.P. (email: jplochocki@midwestern.edu)
Received: 30 March 2017
Accepted: 25 July 2017
Published: xx xx xxxx
OPEN
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
and transversus layer, with muscles in each layer demonstrating a dierent ber orientation (Fig.4). e per-
ineal muscle layers and associated fasciae are continuous with those of the abdomen and thorax. Subcutaneous
muscles of the perineum are present in the same fascial layer as M. cutaneous trunci in the thorax and abdomen.
Fibers of the external layer insert caudally onto an aponeurosis that is continuous with that of the external layer
of the abdomen, M. obliquus externus abdominis, which is continuous with M. intercostales externi in the thorax.
Neurovasculature in the pelvic body wall courses between the internal and transversus layers (e.g., within the
pudendal canal), a pattern observed in the thorax and abdomen where neurovasculature courses between M.
intercostales interni and M. intercostales intimi, and M. obliquus internus abdominis and M. transversus abdominis,
respectively. Endopelvic fascia covering the internal surface of the transversus layer of the pelvis is continuous
with transversalis fascia of the abdomen and endothoracic fascia of the thorax.
e perineal subcutaneous layer includes the M. sphincter ani externus pars subcutanea and M. constrictor
vulvae (variably present) in mammals we dissected (Fig.3). e external layer is comprised of the muscle sheet
associated with the phallus, which is traditionally divided into M. bulbospongiosus, M. ischiocavernosus and M.
transversus perinei supercialis. M. sphincter ani externus pars supercialis is comprised of bers of the M. bul-
bospongiosus portion of the muscle sheet that continues dorsally, continuous with M. sphincter ani externus pars
supercialis, to form a muscular ring. e internal muscle layer is formed by M. sphincter ani externus pars pro-
fundus and its continuity with M. levator ani. e M. transversus perinei profundus, only consistently present
in males, is also part of the internal layer and its bers intermingle with those of M. sphincter ani externus pars
profundus. is layer also includes the urethral sphincter muscles. e transversus layer is comprised of M. levator
ani and M. coccygeus. e portion of M. levator ani most closely associated with the anal canal, M. puborectalis, is
continuous with the deepest edge of M. sphincter ani externus pars profundus. ese ndings suggest M. sphincter
ani externus is not a single muscle, but rather a composite of several muscle layers19, 20. Because of the notable
continuities between M. levator ani and M. sphincter ani externus, these muscles have also been described as con-
tinuous with one another, and even as a single, multi-layered muscle21–23.
Histological sections of the perinea of the adult dog and bovine fetus 15 weeks gestation age similarly demon-
strate four layers of the ventrolateral abdomen and perineal body wall (Fig.4). ese ndings agree with other
histological studies of perineal development that show embryological continuities among muscles in each of
the four trunk layers and separation of the muscle layers by fascial layers during fetal development24, 25. Human
fetuses at roughly 13 weeks of development show continuities between the external muscle layer containing M.
ischiocavernosus, M. bulbospongiosus, and the pars supercialis of the developing M. sphincter ani externus, just
inferior to M. levator ani of the transversus layer26–28. is relationship arises shortly aer the cloacal membrane
obliterates during urogenital septation and remains in the adult29, 30. At this time, M. sphincter ani externus sur-
rounds the anal canal, forming a column extending to the ectoderm-derived epithelium30. Also around the same
time in development, the urinary sphincter muscles become well dened in the internal layer, positioned inferior
to the inferior margin of M. levator ani of the transversus layer but superior to M. bulbospongiosus of the external
layer31. Separations between muscles in each layer form later in development via apoptosis of muscle bers32.
us, the muscle layering found in dissection appears histologically subsequent to embryologic septation of the
cloaca.
e primitive vertebrate characteristic of two ventrolateral body wall muscle layers was expanded in number
and in distribution in the trunk multiple times in vertebrate evolution: at the tetrapod node to four layers in the
thorax and abdomen, and again at the mammal node to four layers throughout the trunk, including the perineum
(Fig.1). Mammalian perineal muscular patterning is associated with the complete septation of the cloaca, which
Figure 1. Cladogram of major vertebrate classes demonstrating the evolution of ventrolateral body wall muscle
layers. Primitively, vertebrates have two ventrolateral muscle layers, while most tetrapods have four layers in the
thorax and abdomen. Mammals exhibit four layers throughout the trunk, including the perineal portion of the
body wall.
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
led to novel anatomical adaptations in mammals relative to other vertebrates. Specically, mammals alone among
vertebrates evolved the suite of characteristics from the anorectal and urogenital chambers formed by cloacal sep-
tation including the rectum, anal canal, urethra, and paired vascular erectile tissues. Other vertebrate intromis-
sion structures, such as those variably found in some sh, lizards, turtles, crocodilians, and waterfowl, arise from
the cloacal wall and have either a single vascular erectile body or one engorged with lymph, and are not homol-
ogous to mammalian genitalia33–35. Lizards, crocodilians, birds, and even monotremes have muscular sphincters
that regulate opening of the cloaca9, 11, 36. ese cloacal muscles, as well as perineal muscles in mammals, were
proposed to evolve from abdominal trunk muscles in previous studies37, 38. However, anatomic, embryonic, and
molecular investigations indicate that, while cloacal muscle precursors temporarily reside in the limb, they later
Figure 2. Muscles of the ventrolateral body wall in the vertebrate abdomen derived from the embryonic
hypaxial and epaxial masses. (A) In shes, such as teleosts, hypaxial muscles of the ventrolateral wall are
organized into two layers (M. obliquus superioris and M. obliquus inferioris). (B) Amphibians, such as
salamanders, have two to four layers (M. obliquus externus, in some species divided into supercialis and
profundus portions, M. obliquus internus, and M. transversus abdominis, with scattered subcutaneous skeletal
muscle bers). (C) Mammals, like dogs, consistently have four layers (M. cutaneous trunci, a well-developed
subcutaneous muscle layer, M. obliquus externus abdominis, M. obliquus internus abdominis and M. transversus
abdominis). Development of the ventral musculature, such as M. rectus abdominis, is regulated by dierent
molecular signals and therefore follows a dierent organizational pattern and may not dierentiate into multiple
layers12.
Figure 3. Anatomical organization of the perineal portion of the mammalian trunk body wall into four layers,
drawn here aer our human dissections. e subcutaneous layer is formed by M. sphincter ani externus pars
subcutanea. e external layer includes M. bulbospongiosus, M. ischiocavernosus and M. transversus perinei
supercialis. e internal muscle layer is formed by M. sphincter ani externus pars profundus, M. transversus
perinei profundus, and the urethral sphincter muscles. e transversus layer includes M. levator ani and M.
coccygeus.
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
migrate to the caudal trunk where they are subjected to the same developmental signaling that regulates trunk
muscular layering to form an extended myotomal sheet similar to that of developing trunk body wall muscles10,
25, 39–42. is may explain why congenital malformations aecting ventrolateral abdominal body wall musculature
are commonly accompanied by perineal muscular defects43, 44.
Evolutionary restructuring of mammalian perineal musculature may be a consequence of interactions
between muscle precursors and connective tissue during musculoskeletal patterning. Skeletal muscles originate
from undierentiated tissue known as the epaxial and hypaxial masses, which give rise to dorsal and ventral body
wall muscles, respectively. Hypaxial muscle cell precursors from the ventrolateral lip of somitic myotomes migrate
through the lateral somitic frontier, i.e., from the primaxial mesodermal domain into the abaxial mesodermal
domain, to populate the ventral body wall, where they are inuenced by connective tissue derived from the lateral
plate45, 46. Developmental signals expressed in lateral plate mesoderm that result in layering of the abdominal
wall also control muscle layering in the perineum, discrete from hindlimb signaling, and are further directed by
local signals that ne-tune muscle development25, 42, 47. Variations in these interactions, along with the modular
property of mesodermal domains, have been used to explain regional dierences in anatomic musculoskeletal
structure across related taxa48, 49. Such anatomic restructuring may also explain similarities of perineal muscle
layering with that of the abdomen and thorax, as cloacal sphincter muscles adapted to specialized reproductive
and excretory functions in mammals. With the evolutionary establishment of the mammalian perineum, somatic
musculature associated with the derived perineal structures was recongured into four layers16. From supercial
to deep, these four muscle layers are (1) the subcutaneous layer, which regulates orice closure, (2) the external
layer, which supplements both erectile and micturition function, (3) the internal layer, which provides primary
Figure 4. Perineum of an adult dog in (A) gross dissection (le lateral view, scale bar 5 mm) and (B)
histological section (le lateral view, scale bar 5 mm). Histological sections of a fetal bovine aged 15 weeks
of the (C) ventrolateral abdominal wall (le anterior view, scale bar 50 µm) and (D) perineum (le lateral
view, scale bar 2 mm). Structures labeled 1–4 are 1, subcutaneous layer; 2, external layer; 3, internal layer;
and 4, transversus layer. Perineal muscle bers (B and D) of the subcutaneous layer (1) are shown in cross-
section, ber orientation in the internal and external layers (2 and 3) is oblique, and ber orientation in the
transversus layer (4) is longitudinal in the taxa that have an anus that is shied to protrude posteriorly, such as
the bovine, dog, and horse, but is transverse in other taxa. e fetal muscle layers (D) are closely associated with
smooth muscle of the internal anal sphincter and rectum (*) and developing sacral vertebrae (◊). a, artifact; i,
integument; SCV, M. sacrocaudalis ventralis, a muscle that acts on the tail.
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
micturition and defecation regulation, and (4) the transversus layer, which provides structural support for pelvic
organs (Fig.3)50.
Our research denes for the rst time the four serially homologous trunk ventrolateral body wall layers in the
perineum. Our sample consists of primates and domestic mammals that represent a broad distribution of placen-
tal mammalian groups that are not closely related phylogenetically, including perissodactyls (horse), artiodactyls
(cow, goat, pig), carnivorans (cat, dog) and primates (human, monkey, prosimian) and form a robust sample from
which to draw conclusions about perineal morphology14. We suggest the primitive anatomical building blocks
and developmental signaling used to construct the thoracic and abdominal trunk body wall were repurposed
in the perineum. Mammalian perineal structure derived from cloacal septation is an evolutionary innovation
that allows for myriad anatomical congurations, diverse reproductive strategies, and precise excretory control
available only to mammals.
Methods
We dissected pelvic and perineal musculature in a subset of adult mammals (Table1). is sample was obtained
from Midwestern University teaching collections, the Arizona Research Collection for Integrative Vertebrate
Education and Study (ARCIVES) housed at Midwestern University (Glendale, AZ, USA), and donated human
cadavers from the National Body Donor Program (St. Louis, MO, USA). All animals in the study were treated in
accordance with the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health with
approval from the Institutional Animal Care and Use Committee at Midwestern University. All human cadavers
were obtained and studied with informed consent and treated in accordance with local and national laws and
regulations with approval from Midwestern University. All muscles of the perineum were dissected according
to methods described in Hall and Walters51. We identied the following perineal muscles during dissection: M.
coccygeus, M. levator ani, M. bulbospongiosus, M. ischiocavernosus, M. transversus perinei supercialis and profun-
dus, M. sphincter ani externus and its subdivisions, and urinary sphincters. During dissection, we observed the
layering, attachment and innervation of each muscle. Histological sections 5 µm thick were taken from the peri-
neum and abdomen of an adult dog and a fetal cow aged 15 weeks of an approximately 40-week gestation period.
Sections were stained with hematoxylin and eosin and imaged under light microscopy.
References
1. Carroll, S. B. Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479–485 (1996).
2. Bure, A. C. & Nowici, J. L. A new view of patterning domains in the vertebrate mesoderm. Dev. Cell. 4, 159–165 (2003).
3. Windner, S. E. et al. Distinct modes of vertebrate hypaxial muscle formation contribute to the teleost body wall musculature. Dev.
Genes Evol. 221, 167–178 (2011).
4. Carrier, D. . Activity of the hypaxial muscles during waling in the lizard Iguana iguana. J. Exp. Biol. 152, 453–470 (1990).
5. Deban, S. M. & Schilling, N. Activity of trun muscles during aquatic and terrestrial locomotion in Ambystoma maculatum. J Exp.
Biol. 212, 2949–2959 (2009).
6. itter, D. Axial muscle function during lizard locomotion. J. Exp. Biol. 199, 2499–2510 (1996).
7. Omura, A. et al. Locomotion pattern and trun musculoseletal architecture among Urodela. Acta Zool. 96, 225–235 (2015).
8. O’eilly, J. C., Summers, A. P. & itter, D. A. e evolution of the functional role of trun muscles during locomotion in adult
amphibians 1. Am. Zool. 40, 123–135 (2000).
9. Eggeling, H. Die Museln des Becenausganges in Handbuch der vergleichenden Anatomie der Wirbeltiere, Bd. 6 (eds Bol, L.,
Göppert, E., allius, E. & Lubosch, W.) 351–374 (Urban und Schwarzenberg, Berlin, 1933).
10. Nishi, S. 1938. Museln des umpfes in Becenausganges in Handbuch der vergleichenden Anatomie der Wirbeltiere, Bd. 6 (eds Bol,
L., Göppert, E., allius, E. & Lubosch, W.) 351–446 (Urban und Schwarzenberg, Berlin, 1938).
11. omer, A. S. Crocodilian pelvic muscles and their avian and reptilian homologues. Bull. Am. Mus. Nat. Hist. 48, 533–552 (1923).
12. Wilson-awls, J., Hurt, C. ., Parsons, S. M. & awls, A. Dierential regulation of epaxial and hypaxial muscle development by
paraxis. Dev. 126, 5217–5229 (1999).
13. Oyama, J. A comparative study on the form of the trun-musculature of cyclostomes. Zool. Mag. 31, 240–244 (I), 261–268 (II),
316–323 (III) (1919).
14. Sisson, S. e anatomy of the domestic animals. (WB Saunders Company, Philadelphia, 1975).
15. Gredler, M. L. et al. Evolution of external genitalia: insights from reptilian development. Sex. Dev. 8, 311–326 (2014).
16. Hynes, P. J. & Fraher, J. P. e development of the male genitourinary system. I. e origin of the urorectal septum and the formation
of the perineum. Br. J. Plast. Surg. 57, 27–36 (2004).
Family Species Common name N
Hominidae Homo sapiens Human 43
Callitrichidae Saguinus oedipu s Cotton-top tamarin 2
Indriidae Propithecus verreauxi Verreaux’s sifaka 2
Lemuridae Lemur catta Ring-tailed lemur 1
Lorisidae Perodicticus potto Potto 1
Equidae Equus caballus Horse 3
Bovidae Capra hircu s Goat 9
Bovidae Bos tauru s Cow 1
Suidae Sus domesticus Pig 9
Canidae Canis familiar is Dog 21
Felidae Felis catus Cat 6
Gallidae Gallus domesticus Chicken 1
Table 1. Sample used in our study.
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Scientific RepoRts | 7: 9182 | DOI:10.1038/s41598-017-09359-y
17. S eifert, A. W., Harfe, B. D. & Cohn, M. J. Cell lineage analysis demonstrates an endodermal origin of the distal urethra and perineum.
Dev. Biol. 318, 143–152 (2008).
18. Mo, . et al. Anorectal malformations caused by defects in sonic hedgehog signaling. Am J Pathol. 159, 765–774 (2001).
19. Santorini, G.D. Anatomici summi septemdecim tabulae. (egia Typographica, Parma, 1775).
20. Sha, A. A new concept of the anatomy of the anal sphincter mechanism and the physiology of defecation. e external anal
sphincter: a triple-loop system. Invest. Urol. 12, 412–9 (1975).
21. Ayoub, S. F. Anatomy of the external anal sphincter in man. Acta Anat. 105, 25–36 (1979).
22. Bogdu, N. Issues in anatomy: e external anal sphincter revisited. Aust. NZ. J. Surg. 66, 626–629 (1996).
23. Lessha, P. Grundlagen der theoretichen Anatomie. (Mason, Leipzig, 1892).
24. Araawa, T. et al. D evelopment of the external anal sphincter with special reference to intergender dierence: observations of mid-
term fetuses (15–30 wees of gestation). Okajimas Folia Anat. Jpn. 87, 49–58 (2010).
25. Valase, P. et al. A dual fate of the hindlimb muscle mass: cloacal/perineal musculature develops from leg muscle cells. Dev. 132,
447–458 (2005).
26. Araawat, T. et al. Development of the external anal sphincter with special reference to intergender dierence: Observations of mid-
term fetuses (15–30 wees of gestation). Okajimas Fol Anat Jap 87, 49–58 (2010).
27. Jin, Z. W. et al. Perineal raphe with special reference to its extension to the anus: a histological study using human fetuses. Anat. Cell
Biol. 49, 116–124 (2016).
28. inugasa, Y. et al. Female longitudinal anal muscles or conjoint longitudinal coats extend into the subcutaneous tissue along the
vaginal vestibule: a histological study using human fetuses. Yonsei Med. J. 54, 778–784 (2013).
29. Sha, A., El Sibai, O., Sha, A. A. & Sha, I. A. A novel concept for the surgical anatomy of the perineal body. Dis. Colon Rectum
50, 2120–2125 (2007).
30. Yamaguchi, ., iyoawa, J. & Aita, . Developmental processes and ectodermal contribution to the anal canal in mice. Ann. Anat .
190, 119–128 (2008).
31. Masumoto, H. et al. eappraisal of intergender dierences in the urethral striated sphincter explains why a completely circular
arrangement is dicult in females: a histological study using human fetuses. Anat. Cell Biol. 45, 79–85 (2012).
32. Chen, Q. J. et al. Apoptosis during the development of pelvic oor muscle in anorectal malformation rats. J Pediatr. Surg. 44,
1884–1891 (2009).
33. Herrera, A. M., Shuster, S. G., Perriton, C. L. & Cohn, M. J. Developmental basis of phallus reduction during bird evolution. Cur r.
Biol. 23, 1065–1074 (2013).
34. Hunter, . H. F. Sex determination, differentiation, and intersexuality in placental mammals. (Cambridge University Press,
Cambridge, 1995).
35. elly, D. A. e functional morphology of penile erection: tissue designs for increasing and maintaining stiness. Integr. Comp. Biol.
42, 216–221 (2002).
36. Farmer, C. G. & Carrier, D. . Pelvic aspiration in the American alligator (Alligator mississippiensis). J. Exp. Biol. 203, 1679–1687
(2000).
37. Eggeling, H. Z. Morphologie der Dammmusulatur. Morph. Jahrb. 24, 405–631 (1896).
38. Johnson, F. P. e development of the rectum in the human embryo. Am. J. Anat. 16, 1–57 (1914).
39. Aita, . An anatomical investigation of the muscles of the pelvic outlet in Japanese giant salamander (Cryptobranchidae
Megalobatrachus japonicus) with special reference to their nerve supply. Ann. Anat . 174, 235–243 (1992).
40. Aita, ., Saamoto, H. & Sato, T. Muscles of the pelvic outlet in the fowl (Gallus gallus domesticus) with special reference to their
nerve supply. J. Morphol. 214, 179–185 (1992).
41. Aita, ., Saamoto, H. & Sato, T. Muscles of the pelvic outlet in the rhesus money (Macaca mulatta) with special reference to
nerve supply. Anat. Rec. 241, 273–283 (1995).
42. ehimi, . et al. A novel role of CXC4 and SDF1 during migration of cloacal muscle precursors. Dev. Dynam. 239, 1622–1631
(2010).
43. ByronScott, . et al. A populationbased study of abdominal wall defects in South Australia and Western Australia. Paediatr.
Perinat. Epidemiol. 12, 136–151 (1998).
44. Hartwig, N. G. et al. Abdominal wall defect associated with persistent cloaca: the embryologic clues in autopsy. Am. J. Clin. Pathol.
96, 640–647 (1991).
45. Cinnamon, Y., ahane, N. & alcheim, C. Characterization of the early development of specific hypaxial muscles from the
ventrolateral myotome. Dev. 126, 4305–4315 (1999).
46. Winslow, B. B., Taimotoimura, . & Bure, A. C. Global patterning of the vertebrate mesoderm. Dev. Dyn. 236, 2371–2381
(2007).
47. Ipulan, L. A. et al. Nonmyocytic androgen receptor regulates the sexually dimorphic development of the embryonic bulbocavernosus
muscle. Endocrinol. 155, 2467–2479 (2014).
48. Shearman, . M. & Bure, A. C. e lateral somitic frontier in ontogeny and phylogeny. J. Exp. Zool. B. Mol. Dev. Evol. 312, 603–612
(2009).
49. Wotton, .., Schubert, F.. & Dietrich, S. In Vertebrate Myogenesis. Hypaxial muscle: controversial classication and controversial
data? pp. 25–48 (Berlin Heidelberg: Springer, 2015).
50. Plochoci, J. H., odriguez-Sosa, J. ., Adrian, B., uiz, S. A. & Hall, M. I. A functional and clinical reinterpretation of human
perineal neuromuscular anatomy: Application to sexual function and continence. Clin. Anat. 29, 1053–1058 (2016).
51. Hall, M. I. & Walters, L. M. An alternate dissection approach to the female urogenital triangle. Clin. Anat. 26, 751–754 (2013).
Acknowledgements
We thank Drs K. Baab, S. Dobson, A. Grossman, W. Grow, C.P. Heesy, K. Muldoon, H. Smith, and J.
VandenBrooks for discussions about the anatomy, S. Ruiz who assisted with dissection preparation, A. Bergeron
for access to specimens, and M. Neumann for assistance with Figure 4. is is Midwestern University Arizona
Research Collection for Integrated Vertebrate Education and Study (ARCIVES) Publication #2. Lastly, we thank
the human cadaveric donors and their families.
Author Contributions
J.H.P., J.R.R-S., and M.I.H. formulated the study design, performed the dissections, and conducted the analyses.
J.H.P. wrote the original dra of the manuscript and J.R.R-S. and M.I.H. contributed to revisions. All authors
approved the nal version and may be held accountable for the work.
Additional Information
Competing Interests: e authors declare that they have no competing interests.
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... In this study the lateral and ventral abdominal anatomy of female capybaras has been described to promote better surgical procedures for sterilization surgeries. The anatomy of the capybaras' abdominal wall followed the general stratigraphy described for mammals [21], with variations concerning the thickness of the skin and cutaneous muscle as well as the distribution of muscular aponeurosis and facility of linea alba identification with a ventral approach, when compared to dogs and horses [22,23]. In agreement with our findings, the abdominal muscles of guinea pigs (Cavia porcellus), hystricomorph ...
... In this study the lateral and ventral abdominal anatomy of female capybaras has been described to promote better surgical procedures for sterilization surgeries. The anatomy of the capybaras' abdominal wall followed the general stratigraphy described for mammals [21], with variations concerning the thickness of the skin and cutaneous muscle as well as the distribution of muscular aponeurosis and facility of linea alba identification ...
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... The thoracic, abdominal, and pelvic wall muscles have three layers (Nishi, 1938;Hall et al., 2017). The traditional view of the homology of muscles between the thoracic and abdominal walls is that the external intercostal muscles correspond to the external oblique abdominis, the inner intercostal muscles to the internal oblique abdominis, and the innermost intercostal muscles to the transverse abdominis (Figures 14A, C). ...
... The thoracolumbar fascia invests the intrinsic back muscles and quadratus lumborum, and the external oblique abdominis muscle is located entirely external to the thoracolumbar fascia ( Figure 14D; Willard et al., 2012;Standring, 2015). Hall et al. (2017) previously documented a homology of the muscular organization between the pelvic and abdominal regions in the body wall. We here provide a different view of muscle homology between the pelvic and thoracic regions, based on the innervation patterns of the different classes of nerve branches. ...
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Due to its long history, the study of human gross anatomy has not adequately incorporated modern embryological findings; consequently, the current understanding has often been incompatible with recent discoveries from molecular studies. Notably, the traditional epaxial and hypaxial muscle distinction, and their corresponding innervation by the dorsal and ventral rami of the spinal nerve, do not correspond to the primaxial and abaxial muscle distinction, defined by the mesodermal lineages of target tissues. To resolve the disagreement between adult anatomy and embryology, we here propose a novel hypothetical model of spinal nerve ramification. Our model is based on the previously unknown developmental process of the intercostal nerves. Observations of these nerves in the mouse embryos revealed that the intercostal nerves initially had superficial and deep ventral branches, which is contrary to the general perception of a single ventral branch. The initial dual innervation pattern later changes into an adult-like single branch pattern following the retraction of the superficial branch. The modified intercostal nerves consist of the canonical ventral branches and novel branches that run on the muscular surface of the thorax, which sprout from the lateral cutaneous branches. We formulated the embryonic branching pattern into the hypothetical ramification model of the human spinal nerve so that the branching pattern is compatible with the developmental context of the target muscles. In our model, every spinal nerve consists of three components: (1) segmental branches that innervate the primaxial muscles, including the dorsal rami, and short branches and long superficial anterior branches from the ventral rami; (2) plexus-forming intramural branches, the serial homolog of the canonical intercostal nerves, which innervate the abaxial portion of the body wall; and (3) plexus-forming extramural branches, the series of novel branches located outside of the body wall, which innervate the girdle and limb muscles. The selective elaboration or deletion of each component successfully explains the reasoning for the standard morphology and variability of the spinal nerve. Therefore, our model brings a novel understanding of spinal nerve development and valuable information for basic and clinical sciences regarding the diverse branching patterns of the spinal nerve.
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... The Pubocaudal muscle group gives rise to the levator ani and ischio-coccygeal muscle, pubourethral-bladder-uterus-rectosacral ligament and Gegenbauer group, after the descent of the genito-urinary septum forms the urethral and anal sphincter muscles and the superficial and deep transverse muscles, bulbocavernosus, and ischiocavernosus [5]. In fetus, these structures are present as a unit, synergistic in their functions. ...
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Female perineum is the tissue complex between the peritoneum and the skin that closes the pelvis inferiorly and its functionality depends on the interplay between organs, tissues, septae and spaces in it. It is a diamond-shaped region below the pelvic floor and extends between the pelvic diaphragm and the perineal skin. It is a surprisingly dynamic field with new insights, discoveries, and controversies and carries differences in viewpoint among anatomists and surgeons. This book chapter will provide an overview regarding perineal anatomy in the female and will focus on embryology, anatomy of the perineal region with modern proponents. It includes detailed anatomy of Urogenital and Anal triangles, their muscles with blood supply and innervation, anatomy and functions of the perineum, its role in Pelvic Organ Prolapse and clinical significance in urinary and fecal incontinence and contribution towards common obstetric and gynecological pathologies.
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... The tetrapods comprise four-limbed animals and is the superclass containing the four subclasses of mammals, amphibians, birds and reptiles. As these animals further evolved, differentiating themselves from fish and the other animal classes, the anatomy of their abdominal walls began to follow a similar framework [24]. Such that, within mammals, the general structure of the abdominal wall is largely conserved. ...
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Purpose With the increased use of simulation-based training using animal models for the education of surgical and anaesthetic techniques, an increased understanding of the anatomy of such models and how they compare to humans is required. The transversus abdominis plane block is a regional anaesthetic technique that requires an understanding of the abdominal wall anatomy along with proficient ultrasound use. The current review aims to compare the anatomy of the abdominal wall across species, particularly focussing on the pertinent differences within the class of mammals, and secondarily, it aims to address the implications of these differences for the use of simulation-based training of the transversus abdominis plane block. Methods To achieve this, the PubMed, Web of Science and Google Scholar databases were searched for relevant literature. Studies pertaining to the musculature, vasculature or innervation of the anterolateral abdominal wall across species were included. Results The mammalian abdominal wall differs in its musculature, vasculature or innervation from that of amphibians, birds or reptiles; however, among species of mammals, the structure of the abdominal wall follows a similar framework. Particular differences among mammals include the additional muscular layer of the panniculus carnosus found in most mammals other than humans, the variable arterial origins and dominant vascular supply of the abdominal wall and the number of thoracolumbar nerves innervating the abdominal wall. Conclusion When using animal models for simulation-based training, the pig is recommended for the transversus abdominis plane block given its closely homologous abdominal wall structure, availability and larger comparative size.
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... The tetrapods comprise four-limbed animals and is the superclass containing the four subclasses of mammals, amphibians, birds and reptiles [9]. As these animals further evolved, differentiating themselves from fish and the other animal classes, the anatomy of their abdominal walls began to follow a similar framework [10]. Such that, within mammals, the general structure of the abdominal wall is largely conserved [11]. ...
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With the increased use of simulation based training using animal models for the education of surgical and anaesthetic techniques, an increased understanding of the anatomy of such models and how they compare to humans is required. The transversus abdominis plane block is a regional anaesthetic technique that requires an understanding of the abdominal wall anatomy along with proficient ultrasound use. The current review aims to compare the anatomy of the abdominal wall across species, particularly focussing on the pertinent differences within the class of mammals, and secondarily, it aims to address the implications of these differences for simulation based training of the transversus abdominis plane block. To achieve this, the PubMed, Web of Science and Google Scholar databases were searched for relevant literature. The mammalian abdominal wall differs in its musculature, vasculature or innervation from that of amphibians, birds or reptiles, however, among species of mammals, the structure of the abdominal wall follows a similar framework. Particular differences among mammals include the additional muscular layer of the panniculus carnosus found in most mammals other than humans, the variable arterial origins and dominant vascular supply of the abdominal wall and the number of thoracolumbar nerves innervating the abdominal wall. When using animal models for simulation based training, the pig is recommended for the transversus abdominis plane block given its closely homologous abdominal wall structure, availability and larger comparative size.
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... Innervation patterns in the thoracic and abdominal regions in our model may lead to radical changes of view on the muscle organization of the body wall ( Figure 5). The muscles in the thoracic, abdominal, and pelvic walls have three layers (the cutaneous muscle layer is not counted because of its absence in human; Nishi, 1938, Hall et al., 2017. The traditional view on the homology of muscles between the thoracic and abdominal walls is that the external intercostal muscle corresponds to the external oblique abdominis, the intercostal interni to the internal oblique abdominis, and the intercostal intimi to the transverse abdominis. ...
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... A complete understanding of the reproductive health of dogs is mutually beneficial to the wellbeing of dogs and their owners, as well as being economically and socially important (Wells 2007;Friedmann & Son 2009;Hall et al. 2016). Accurate and complete descriptions of the dog perineum, the anatomical region between the pubic symphysis and caudal vertebrae, are important for understanding the evolution of mammalian reproduction and evolutionary relationships among taxa, as well as for successful breeding and surgical interventions related to infection, perianal fistulas, continence, urethrostomy, ovariohysterectomy, vulvovaginal cancer anal sac pathologies, vaginal prolapse and certain approaches to perineal hernia correction (Ashdown 1968;Vasseur 1984;Bilbrey et al. 1990;Hill et al. 2000;Smeak 2000;Morrison 2002; Ralphs & Kramek 2003;Vnuk et al. 2009;Fossum 2013;Cinti et al. 2015;Hall et al. 2017). ...
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Understanding the homologies between male and female perineal structure helps both evolutionary biologists and clinicians better understand the evolution and anatomy of canines. Domestic dogs (Canis familiaris) play an important role in human society, and canine perineal anatomy is important for maintaining dogs’ reproductive health for successful breeding and a wide variety of pathologies. Here, we investigate homologies between male and female perineal structure, identifying structures based on common function, anatomical relationships and attachments. In this investigation we dissected 21 male and female large‐breed dogs. We find broad structural homologies between male and female dogs related to erection, micturition and defecation, including muscles, fasciae and erectile tissue. Using these homologies will help anatomists and clinicians interpret the anatomical organization of the perineum, a notoriously difficult area of anatomy.
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Evolution of the vertebrate urinary system occurs in response to numerous selective pressures, which have been incompletely characterized. Developing research into urinary evolution led to the occurrence of clinical applications and insights in paediatric urology, reproductive medicine, urolithiasis and other domains. Each nephron segment and urinary organ has functions that can be contextualized within an evolutionary framework. For example, the structure and function of the glomerulus and proximal tubule are highly conserved, enabling blood cells and proteins to be retained, and facilitating the elimination of oceanic Ca+ and Mg+. Urea emerged as an osmotic mediator during evolution, as cells of large organisms required increased precision in the internal regulation of salinity and solutes. As the first vertebrates moved from water to land, acid-base regulation was shifted from gills to skin and kidneys in amphibians. In reptiles and birds, solute regulation no longer occurred through the skin but through nasal salt glands and post-renally, within the cloaca and the rectum. In placental mammals, nasal salt glands are absent and the rectum and urinary tracts became separate, which limited post-renal urine concentration and led to the necessity of a kidney capable of high urine concentration. Considering the evolutionary and environmental selective pressures that have contributed to renal evolution can help to gain an increased understanding of renal physiology.
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Evolution of surrogate light chain in tetrapods and the relationship between lengths of CDR H3 and VpreB tails
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In the mammalian immune system, the surrogate light chain (SLC) shapes the antibody repertoire during B cell development by serving as a checkpoint for production of functional heavy chains (HC). Structural studies indicate that tail regions of VpreB contact and cover the third complementarity-determining region of the HC (CDR H3). However, some species, particularly bovines, have CDR H3 regions that may not be compatible with this HC-SLC interaction model. With immense structural and genetic diversity in antibody repertoires across species, we evaluated the genetic origins and sequence features of surrogate light chain components. We examined tetrapod genomes for evidence of conserved gene synteny to determine the evolutionary origin of VpreB1, VpreB2, and IGLL1, as well as VpreB3 and pre-T cell receptor alpha (PTCRA) genes. We found the genes for the SLC components (VpreB1, VpreB2, and IGLL1) only in eutherian mammals. However, genes for PTCRA occurred in all amniote groups and genes for VpreB3 occurred in all tetrapod groups, and these genes were highly conserved. Additionally, we found evidence of a new VpreB gene in non-mammalian tetrapods that is similar to the VpreB2 gene of eutherian mammals, suggesting VpreB2 may have appeared earlier in tetrapod evolution and may be a precursor to traditional VpreB2 genes in higher vertebrates. Among eutherian mammals, sequence conservation between VpreB1 and VpreB2 was low for all groups except rabbits and rodents, where VpreB2 was nearly identical to VpreB1 and did not share conserved synteny with VpreB2 of other species. VpreB2 of rabbits and rodents likely represents a duplicated variant of VpreB1 and is distinct from the VpreB2 of other mammals. Thus, rabbits and rodents have two variants of VpreB1 (VpreB1-1 and VpreB1-2) but no VpreB2. Sequence analysis of VpreB tail regions indicated differences in sequence content, charge, and length; where repertoire data was available, we observed a significant relationship between VpreB2 tail length and maximum DH length. We posit that SLC components co-evolved with immunoglobulin HC to accommodate the repertoire – particularly CDR H3 length and structure, and perhaps highly unusual HC (like ultralong HC of cattle) may bypass this developmental checkpoint altogether.
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Evolution of External Genitalia: Insights from Reptilian Development
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  • Aug 2014
  • SEX DEV
External genitalia are found in each of the major clades of amniotes. The phallus is an intromittent organ that functions to deliver sperm into the female reproductive tract for internal fertilization. The cellular and molecular genetic mechanisms of external genital development have begun to be elucidated from studies of the mouse genital tubercle, an embryonic appendage adjacent to the cloaca that is the precursor of the penis and clitoris. Progress in this area has improved our understanding of genitourinary malformations, which are among the most common birth defects in humans, and created new opportunities for comparative studies of other taxa. External genitalia evolve rapidly, which has led to a striking diversity of anatomical forms. Within the past year, studies of external genital development in non-mammalian amniotes, including birds, lizards, snakes, alligators, and turtles, have begun to shed light on the molecular and morphogenetic mechanisms underlying the diversification of phallus morphology. Here, we review recent progress in the comparative developmental biology of external genitalia and discuss the implications of this work for understanding external genital evolution. We address the question of the deep homology (shared common ancestry) of genital structures and of developmental mechanisms, and identify new areas of investigation that can be pursued by taking a comparative approach to studying development of the external genitalia. We propose an evolutionary interpretation of hypospadias, a congenital malformation of the urethra, and discuss how investigations of non-mammalian species can provide novel perspectives on human pathologies. © 2014 S. Karger AG, Basel.
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Nonmyocytic Androgen Receptor Regulates the Sexually Dimorphic Development of the Embryonic Bulbocavernosus Muscle
Article
Full-text available
  • Apr 2014
  • ENDOCRINOLOGY
The BC (bulbocavernosus) is a sexually dimorphic muscle observed only in males. ARKO (Androgen receptor knock out) mouse studies show the loss of BC formation. This suggests that androgen signaling plays a vital role in its development. Androgen has been known to induce muscle hypertrophy through satellite cell activation and myonuclei accretion during muscle regeneration and growth. Whether the same mechanism is present during embryonic development is not yet elucidated. To identify the mechanism of sexual dimorphism during BC development, the timing of morphological differences was first established. It was revealed that the BC was morphologically different between male and female mice at E16.5. Differences in the myogenic process were detected at E15.5. The male BC possesses a higher number of proliferating undifferentiated myoblasts. To identify the role of androgen signalling in this process, muscle-specific androgen receptor (AR) mutation was introduced which resulted in no observable phenotypes. Hence, the expression of AR in the BC was examined and found that the AR did not colocalize with any muscle markers such as MyoD, Myog, and Pax7. It was revealed that the mesenchyme surrounding the BC expressed AR and the BC started to express AR at E15.5. AR mutation on the non-myocytic cells utilizing Sall1 (spalt-like transcription factor 1) Cre driver mouse was performed which resulted in defective BC formation. It was revealed that the number of proliferating undifferentiated myoblasts was reduced in the SallAR (Sall1 Cre:AR(L-/Y)) mutant embryos and the adult mutants were devoid of BC. The transition of myoblasts from proliferation to differentiation is mediated by Cdk-inhibitors. An increased expression of p21 was observed in the BC myoblast of the SallAR mutant and WT female. Altogether, this study suggets that the non-myocytic AR may paracrinely regulate the proliferation of myoblast possibly through inhibiting p21 expression in myoblasts of the BC.
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Locomotion pattern and trunk musculoskeletal architecture among Urodela
Article
Full-text available
  • Feb 2014
  • ACTA ZOOL-STOCKHOLM
We comparatively examined the trunk musculature and prezygapophyseal angle of mid-trunk vertebra in eight urodele species with different locomotive modes (aquatic Siren intermedia, Amphiuma tridactylum, Necturus maculosus and Andrias japonicus; semi-aquatic Cynops pyrrhogaster, Cynops ensicauda; and terrestrial Hynobius nigrescens, Hynobius lichenatus and Ambystoma tigrinum). We found that the more terrestrial species were characterized by larger dorsal and abdominal muscle weight ratios compared with those of the more aquatic species, whereas muscle ratios of the lateral hypaxial musculature were larger in the more aquatic species. The lateral hypaxial muscles were thicker in the more aquatic species, whereas the M. rectus abdominis was more differentiated in the more terrestrial species. Our results suggest that larger lateral hypaxial muscles function for lateral bending during underwater locomotion in aquatic species. Larger dorsalis and abdominal muscles facilitate resistance against sagittal extension of the trunk, stabilization and support of the ventral contour line against gravity in terrestrial species. The more aquatic species possessed a more horizontal prezygapophyseal angle for more flexible lateral locomotion. In contrast, the more terrestrial species have an increasingly vertical prezygapophyseal angle to provide stronger column support against gravity. Thus, we conclude trunk structure in urodeles differs clearly according to their locomotive modes.
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The Evolution of the Functional Role of Trunk Muscles During Locomotion in Adult Amphibians
Article
Full-text available
  • Feb 2000
  • Am Zool
SYNOPSIS. The axial musculature of all vertebrates consists of two principal mas- ses, the epaxial and hypaxial muscles. The primitive function of both axial muscle masses is to generate lateral bending of the trunk during swimming, as is seen in most fishes. Within amphibians we see multiple functional and morphological elab- orations of the axial musculature. These elaborations appear to be associated not only with movement into terrestrial habits (salamanders), but also with subsequent locomotor specializations of two of the three major extant amphibian clades (frogs and caecilians). Salamanders use both epaxial and hypaxial muscles to produce lateral bending during swimming and terrestrial, quadrupedal locomotion. How- ever during terrestrial locomotion the hypaxial muscles are thought to perform an added function, resisting long-axis torsion of the trunk. Relative to salamanders, frogs have elaborate epaxial muscles, which function to both stabilize and extend the iliosacral and coccygeosacral joints. These actions are important in the effective use of the hindlimbs during terrestrial saltation and swimming. In contrast, cae- cilians have relatively elaborate hypaxial musculature that is linked to a helix of connective tissue embedded in the skin. The helix and associated hypaxial muscles form a hydrostatic skeleton around the viscera that is continuously used to main- tain body posture and also contributes to forward force production during bur- rowing.
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Sex Determination, Differentiation and Intersexuality in Placental Mammals
Book
  • Mar 1995
How do males become male and females become female? And what are the consequences if the decision is not incisive? Drawing upon interests in animal genetics and molecular biology, the author endeavours to answer these difficult yet fascinating questions. Originally published in 1995, this book describes the genetic determination of sex and examines how sexual organs are differentiated. Using examples of intersexuality, chimaeras and asymmetries, the book describes the underlying molecular basis of sex determination and sexual differentiation, and focuses on the critical role of the rate of embryonic development in these vital processes. Male precocity is a recurrent theme, as is the involvement of Sertoli cells and their secretion of anti-Müllerian hormone. An invaluable book for reproductive physiologists, geneticists and developmental biologists whose interests may extend from animal science through veterinary medicine to human clinical medicine.
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A Functional and Clinical Reinterpretation of Human Perineal Neuromuscular Anatomy: Human perineal anatomy
Article
  • Aug 2016
Introduction: Modern anatomical and surgical references illustrate perineal muscles all innervated by branches of the pudendal nerve but still organized into anatomically distinct urogenital and anal triangles with muscles inserting onto a central perineal body. However, this conflicts with the anatomy commonly encountered during dissection. Materials and Methods: We use dissections of 43 human cadavers to characterize the anatomical organization of the human perineum and compare our findings to standard references. Results: We found bulbospongiosus and the superficial portion of the external anal sphincter (EAS) were continuous anatomically with a common innervation in 92.3% of specimens. The superficial transverse perineal muscle inserted anterior and lateral to the midline, interdigitating with bulbospongiosus. The three EAS subdivisions were anatomically discontinuous. Additionally, in 89.2% of our sample the inferior rectal nerve emerged as a branch of S3 and S4 distinct from the pudendal nerve and innervated only the subcutaneous EAS. Branches of the perineal nerve innervated bulbospongiosus and the superficial EAS and nerve to levator ani innervated the deep EAS. Conclusions: We empirically demonstrate important and clinically relevant differences with perineal anatomy commonly described in standard texts. First, independent innervation to the three portions of EAS suggests the potential for functional independence. Second, neuromuscular continuity between bulbospongiosus and superficial EAS suggests the possibility of shared or overlapping function of the urogenital and anal triangles. This article is protected by copyright. All rights reserved.
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Hypaxial Muscle: Controversial Classification and Controversial Data?
Article
  • Sep 2015
  • Results Probl Cell Differ
Hypaxial muscle is the anatomical term commonly used when referring to all the ventrally located musculature in the body of vertebrates, including muscles of the body wall and the limbs. Yet these muscles had very humble beginnings when vertebrates evolved from their chordate ancestors, and complex anatomical changes and changes in underlying gene regulatory networks occurred. This review summarises the current knowledge and controversies regarding the development and evolution of hypaxial muscles.
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An alternate dissection approach to the female urogenital triangle
Article
  • Sep 2013
  • CLIN ANAT
Traditional dissections of the female urogenital (UG) triangle can lead to early destruction of the erectile tissues, associated musculature, and neurovascular structures. Here, we present an alternate dissection of the female UG triangle. Rather than begin the female UG triangle dissection with the fatty tissue of the labia majora, we utilize an early identification of the suspensory ligament of the clitoris to organize the dissection. The suspensory ligament leads to the body of the clitoris, which can be palpated from distal to proximal to find the crura of the clitoris with overlying ischiocavernosus muscles. Once the crura have been defined, the bulbs of the vestibule with overlying bulbospongiosus muscles can be palpated medially and posteriorly. This dissection approach results in a clean dissection that well demonstrates homologies between male and female external genitalia. Through the use of this method, most student dissection attempts are able to demonstrate the erectile tissues and associated musculature that comprise the female UG triangle. This technique can also be used for male UG triangle dissections, encouraging identification of male and female homologies. Clin. Anat., 2013. © 2013 Wiley Periodicals, Inc.
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