Early Development of the Shoulder Girdle and Sternum in Marsupials (Mammalia: Metatheria)

99 Pages·1987·4 MB·English

by  Prof. Dr. Milan Klima (auth.)

Advances in Anatomy
Embryology and Cell Biology
Vol. 109
Editors
F. Beck, Leicester W Hild, Galveston
W Kriz, Heidelberg R. Ortmann, KOln
J.E. Pauly, Little Rock T.H. Schiebler, Wiirzburg
Milan Klima
Early Development
of the Shoulder Girdle
and Sternum in Marsupials
(Mammalia: Metatheria)
With 33 Figures
Springer-Verlag
Berlin Heidelberg N ewYork
London Paris Tokyo
Prof. Dr. Milan Klima
Anatomisches Institut, Johann Wolfgang Ooethe-Universitat
Theodor-Stern-Kai 7, 6000 Frankfurt am Main, FRO
Granted by Hubrecht Laboratory, International Embryological Institute,
Utrecht and by Deutsche Forschungsgemeinschaft, Bonn
ISBN-13: 978-3-540-18358-7 e-ISBN-13: 978-3-642-72994-2
DOl: 10.1007/978-3-642-72994-2
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Contents
1 Introduction and Review of the Literature 1
2 Material and Methods 3
3 Results 9
3.1 Early Morphogenesis 9
3.1.1 Dasyurus quoll 9
3.1.2 Thylacis obesolus 16
3.1.3 Perameles nasuta 19
3.1.4 Triehosurus vulpeeula 21
3.1.5 Phaseolaretos cinereus 35
3.1.6 Vombatus ursinus 41
3.1.7 Petrogale penicillata 45
3.1.8 Thylogale thetis . 46
3.1.9 Thylogale parma 47
3.1.10 Wallabia dorsalis 47
3.1.11 M aerop us rufus 47
3.2 Conditions in Adults 48
3.2.1 Didelphidae 49
3.2.2 Dasyuridae 49
3.2.3 Notoryctidae 49
3.2.4 Peramelidae 51
3.2.5 Caenolestidae 51
3.2.6 Phalangeridae 51
3.2.7 Vombatidae 53
3.2.8 Macropodidae 53
4 Results and Discussion 54
4.1 Comparison of Shoulder Girdle and Sternal
Structures in Monotremes, Marsupials, and
Placentals 54
4.2 Morphogenesis of Shoulder Girdle and Sternal
Structures in Marsupials 56
4.2.1 Scapula 56
4.2.2 Metacoracoid 57
4.2.3 Procoracoid 59
4.2.4 The First Rib 61
V
4.2.5 Paired Sternal Elements 61
4.2.6 Unpaired Sternal Element 62
4.2.7 Clavicle 65
4.3 Functional Relationships 65
4.3.1 Breast-Shoulder Arch in Marsupial Neonates 65
4.3.2 Movements of Marsupial Neonates at Birth 69
4.3.3 External Morphology of Intrauterine Embryos,
Neonates, and Pouch Young of Marsupials 73
4.4 Evolutionary Relationships 78
5 Summary 81
Acknowledgements 83
References 84
SUbject Index 89
VI
Abbreviations
a acromion
cl clavicle
cs coracoid-scapular plate
g glenoid cavity
h humerus
ic interclavicle
icc pars chondralis interclaviculae (unpaired chondral
element of the interclavicle, unpaired sternal element)
icd pars desmalis interclaviculae (paired desmal element of
the interclavicle)
mc metacoracoid
mst manubrium sterni
os suprasternal ossicle
pc procoracoid
pcl praeclavium
pcs coracoid process
rl,2 ribs 1, 2000
s scapula
st sternum
stb sternebra
stl sternal band (paired sternal element)
VII
1 Introduction and Review of the Literature
This book is related closely to an earlier work on the morphogenesis of the
shoulder girdle and sternum in the egg-laying mammals (Monotremata) which
was also published in Advances in Anatomy, Embryology and Cell Biology (Klima
1973). Some of the problems that have been discussed within this topic remain
relevant to this day. This research on pouch mammals (Marsupialia) will empha
size two aspects especially. First, a comparison with the respective results in
other mammals will be made, and the resulting phylogenetic problems clari
fied. Secondly, the hitherto barely recognized functional relations will be dis
cussed.
Like the earlier publication, this book has relied decisively on investigation
of the extensive Hill Collection from the Hubrecht Laboratory, International
Embryological Institute, Utrecht. More than 100 serial sections from 11 species
were investigated, representing the most complete source material that has ever
been examined for such a purpose. This is the first time that it has been possible
not only to describe the morphogenesis of the marsupial breast-shoulder appara
tus through single developmental stages, but to comprehend it as a continuous
process.
Individual descriptions of the marsupial shoulder girdle and sternum can
be found in the earliest literature dealing with individual species of marsupials.
The first work to summarize this topic was Parker's (1868) monograph on
the shoulder girdle and sternum of vertebrates. However, since only adult and
juvenile marsupials were at his disposal his reflections on comparative anatomy
could not include or refer to the early developmental stages.
Some publications dealing with the connection between the clavicle and
sternum in mammals (Gegenbaur 1864; Goette 1877; Anthony 1898, 1901;
Eggeling 1904, 1906; Ohngren 1919) included some observations on marsupials,
mainly on pouch young and on juvenile specimens of Didelphis. However, these
investigations failed to contribute decisively to the clarification of the morpho
genetic processes in the marsupial breast-shoulder apparatus.
Some basic research on the morphogenesis of the shoulder girdle in marsu
pials has been carried out since the tum of the century. Broom (1897, 1899,
1902, 1912) investigated several early stages of Trichosurus and some early stages
of Dasyurus, Perameles, Pseudocheirus, and Petrogale. He observed" ... at birth
a well developed coracoid which is firmly attached to the sternum" (Broom
1902). This observation was later confirmed by Watson (1917) for Trichosurus,
and Hansen (1920) supplemented it for Didelphis. Romer (1922) considered
all these results in a thorough discussion, and his conclusions form the basis
for the hitherto generally accepted theory on the origin of the coracoid elements
in mammals, which isrepresented in almost all comparative anatomy textbooks.
1
One can find statements specifically about the development of the shoulder
girdle in marsupials only in a few later publications. McCrady (1938) reported
on it in his mono graphical work on the embryological development of Didelphis.
Cheng (1955) offered some statements in connection with his investigations
into the development of the shoulder muscles in Didelphis. Hill and Osman
Hill (1955) reported briefly on the shoulder girdle in connection with their
observations on the anatomy of the newborn young of Dasyurus. McKenna
(1961) compared the marsupial shoulder girdle with that of the extinct mamma
lian order Multituberculata.
The basic reports by Broom (1897,1899,1902,1912), Watson (1917), Han
son (1920), and Romer (1922), as well as the later publications of McCrady
(1938), Cheng (1955), and McKenna (1961), all deal primarily with the lateral
parts of the marsupial shoulder girdle. The medial part, i.e., the sternum and
its individual elements, has barely attracted any attention. Nonetheless, this
part especially plays an important role in the breast-shoulder apparatus. The
mammalian sternum stems embryologically from two paired sternal bands. As
recognized earlier (Gegenbaur 1864; Ruge 1880; Eggeling 1904, 1906; Muller
1906; Ohngren 1919; Gladstone and Wakeley 1932; Reiter 1942), additional
structures add themselves to these elements in the cranial area. The exact mor
phogenesis of these structures has been described only very recently, in investiga
tions both on' humans (Klima 1968a, 1975a, 1976) and on a whole variety
of different mammals (Klima 1967, 1968b, c, 1972, 1973, 1975b, 1978). These
publications include some references to recent observations on marsupials and
reflections about the phylogenetic origin of the mammalian breast-shoulder ap
paratus (Klima 1973, 1975a, b). The results have been compiled into a textbook
on comparative anatomy by Starck (1979). However, a comprehensive treatment
of this topic has not yet been accomplished.
2
2 Material and Methods
The entire material for the investigation of early development came from the J.P. Hill Collec
tion, now in the Hubrecht Laboratory, International Embryological Institute, Utrecht. All
in all, 109 histological series from 11 marsupial species proved useful for the subject of the
present paper. The objects were cut transversely and sagittally. Azan staining was applied
to most of the histological series, whereas hematoxylin and eosin (H & E) staining was used
for only some of them.
The individual developmental stages of the material were originally labelled very differently
in the collections and in the notebooks of J.P. Hill: "embryo," "uterine embryo," "intra
uterine embryo," "shortly before birth," "just born," "new-born embryo," "new-born
young, " "recently born young," "unattached young," attached young, " "mammary foetus, "
"young, " "pouch young, " and" free pouch young. " These terms are also found in the publica
tions of Hill and 'his assistants (Hill 1898, 1901, 1910, 1918; Fraser and Hill, 1915; Hill
and Osman Hill 1955); they have not always been used consistently. For the purposes of
the present paper, they had to be simplified and standardized. With reference to the current
terminology in the most recent literature on the Marsupialia (Tyndale-Biscoe 1973; Hunsacker
1977; Hunsacker and Shupe 1977; Millar 1977, 1981; Case 1978; Cutts et al. 1978; Lillegraven
1979, 1984, 1985; Archer 1982; Russel 1982a, b; Nowak and Paradiso 1983), I have divided
the stages of development investigated into three main groups and named them as follows:
intrauterine embryo, neonate, and pouch young.
In the collection and also in the notebooks of J.P. Hill, the size of the intrauterine embryos,
neonates, and pouch young is given in millimeters for greatest length (OL), head length (HL),
and dorsal curve length (DCL). In this paper, only the OL dimension is used, "measured
in the curved attitude from anterior extremity of head to rounded posterior end of body"
(Hill and Osman Hill 1955). This size label corresponds to the current term "crown-rump
length" (CR).
The external morphology of many intrauterine embryos, neonates, and pouch young was
documented by J.P. Hill with drawings and photographs. The documents are contained in
J.P. Hill's notebooks, which form part of the Hill Collection. The collection also contains
some detailed pencil drawings by A. Cronin of Sydney, only a few of which have as yet
been published (Hill and Osman Hill 1955). For the purposes of this paper, I have made
some outline drawings of selected developmental stages, based on these originals (Figs. 32,
33). The unpublished drawings by A. Cronin can be found elsewhere (Klima and Bangma
1987).
The observations on all the objects were recorded. Drawings and photographs of selected
cross sections were made and thus integrated into the record. Reconstructions of the breast
shoulder apparatus of some developmental stages of Dasyurus quol!, Thylacis obesolus, Phasco
larctos cinereus, Vombatus ursinus, and Thylogale thetis were drawn. Eight of the most impor
tant developmental stages of Trichosurus vulpecula were selected for the construction of plastic
models. The models were constructed according to the same photographic method as that
described in an earlier paper on monotremes (Klima 1973).
For a precise description of the conditions in adults, it was necessary to investigate only
completely conserved skeletons in which the natural connections between the various parts
of the breast-shoulder apparatus had not been destroyed by preparatory techniques. Such
material is quite rare. I was able to evaluate material for that purpose which originated from
the following institutions: Institut voor Taxonomische Zoo logie, Amsterdam; Naturmuseum
Senckenberg, Frankfurt am Main; British Museum (Natural History), London; Museum Na
tional d'Histoire Naturelle, Paris; Staatliches Museum fUr Naturkunde, Stuttgart. It proved
3
Table 1. Survey of the marsupial material examined
Specimens
Histo- Osteo-
logical logical
(n) (n)
Didelphidae
Marmosa murina (Linne 1758), murine opossum 0 2
Metachirops opossum (Linne 1758), four-eyed opossum 0 3
Chironectes minimus Zimmermann 1780, water opossum 0
Didelphis marsupialis Linne 1758, common opossum 0 4
Dasyuridae
Dasyurus quol! Zimmermann 1977, in Hill Collection labelled as Dasyurus
viverrinus, Eastern dasyure 32 3
Dasyurus maculatus (Kerr 1792), spotted-tailed dasyure o
Sacrophilus harrisi (Boitard 1841), Tasmanian devil o 2
Notoryctidae
Notoryctes typhlops (Stirling 1889), marsupial mole o
Peramelidae
Thylads obesolus (Shaw and Nodder 1797), in Hill Collection labelled
as Perameles obesula, Southern short-nosed bandicoot 8 4
Perameles nasuta Geoffroy 1804, long-nosed bandicoot 3
Caenolestidae
Lestoros inca (Thomas 1917), Incan "rat" opossum o
Phalangeridae
Trichosurus vulpecula (Kerr 1792), brush-tailed phalanger 40 6
Phalanger gymnotis (Peters and Doria 1875), cuscus o
Petaurus breviceps Waterhouse 1839, honey glider o 2
Petaurus australis Shaw and N odder 1791, yellow-bellied glider o 2
Pseudocheirus lemuroides (Collett 1884), brush-tipped ring tail o 3
Phascolarctos dnereus (GoldfuB 1817), koala 12 3
Vombatidae
Vombatus ursinus (Shaw 1800), in Hill Collection labelled as Phascolomys
mitchelli, common wombat 5
M acropodidae
Aepyprymnus rufescens (Gray 1837), rufous rat kangaroo o 1
Petrogale penicillata (Griffith 1827), brush-tailed rock wallaby 5
Dendrolagus ursinus Temminck 1836, black tree kangaroo o 1
Thylogale thetis (Lesson 1828), red-necked pademelon 2 o
Thylogale stigmatica Gould 1860, red-legged pademelon o 2
Thylogale parma (Waterhouse 1846), in Hill Collection labelled as Wal!a
bia parma, Parma wallaby o
4