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PubMed2003

The marsupial placenta: a phylogenetic analysis.

The structure, physiology, and endocrinology of the yolk sac placenta of different marsupial groups is compared and phylogenetically analyzed to provide information on placental characters in the marsupial stem species. We conclude that the marsupial stem species possessed a functional yolk sac placenta. Histotrophic nutrition by uterine secretion decreased during late pregnancy and at least half of the yolk sac was vascularized at the time of shell coat rupture. Due to yolk sac fusion, the larger part of the avascular, bilaminar yolk sac could not serve as a placenta at late gestation in the polyovular marsupial stem species. The bilaminar yolk sac gained a relatively greater importance for nutrition in monovular australidelphians. In macropodids a greater proportion of the yolk sac remained bilaminar at the time of shell coat rupture than in the stem species. Another derived feature of macropodids is the sustained plasma progesterone synthesis that is in turn responsible for an extended secretory phase of the uterus and a lengthened gestation. The placenta of the marsupial stem species was probably capable of metabolising histo- and hemotrophes. Recognition of pregnancy during early stages of development is a derived character of macropodids that we suggest did not occur in the marsupial stem species. However, birth and birth behaviour were apparently induced by prostaglandins in the marsupial stem species. Although the yolk sac formed the definitive placenta, it is likely that the allantois provided a supplementary placental function in the marsupial stem species, but that the role of the allantois became progressively less important during the evolution of marsupial placentation.

Animals↗
PubMed2003

Functional-adaptive anatomy of the axial skeleton of some extant marsupials and the paleobiology of the paleocene marsupials Mayulestes ferox and Pucadelphys andinus.

In this study, the axial skeletons of two Early Paleocene marsupials, Mayulestes ferox and Pucadelphys andinus, were analyzed functionally and compared to that of six South American and three Australian species of extant marsupials. In the case of the South American opossums, myological data of the epaxial musculature were collected and analyzed and osteological-myological associations were related to locomotor behavior. Various features of the vertebral column that relate to diet or to locomotor or postural patterns were pointed out. These features include: the craniocaudal development of the neural process of the axis; the position of the anticlinal vertebra; the morphology of the neural processes of the thoracolumbar vertebrae (orientation, length, and craniocaudal width); the length, orientation, and curvature of the transverse processes of the lumbar vertebrae; and the length and robustness of the caudal vertebrae. In both fossil forms the vertebral column is mobile and allows a great range of flexion and extension of the spine, more so than in most of the living didelphids. It is emphasized here that the analysis of the axial skeleton complements and improves the conclusions provided by the forelimb and hindlimb analyses. It is proposed that Mayulestes and Pucadelphys represent an ancestral morphotype suggesting that the generalized type of locomotion of Paleocene marsupials was partly terrestrial with some climbing ability.

Adaptation, Physiological↗
PubMed2003

Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula.

The development of the scapula was studied in embryonic and postnatal specimens of Monodelphis domestica and perinatal specimens of Philander opossum, Caluromys philander, and Sminthopsis virginiae using histological sections and 3D reconstructions. Additionally, macerated skeletons of postnatal M. domestica were examined. This study focused on the detachment of the scapulocoracoid from the sternum and on the acquisition of a supraspinous fossa, a supraspinatus muscle, and a scapular spine, all these events associated with the origin of the therian shoulder girdle. In none of the specimens is there a continuity of the cartilaginous scapulocoracoid with the sternum, even though the structures are in close proximity, especially in S. virginiae. At birth, the first rib laterally presents a pronounced boss that probably contacts the humerus during certain movements. Only the acromial portion of the scapular spine, which originates from the anterior margin of the scapular blade, is preformed in cartilage. The other portion is formed by appositional bone ("Zuwachsknochen"), which expands from the perichondral ossification of the scapula into an intermuscular aponeurosis between the supra- and infraspinous muscles. This intermuscular aponeurosis inserts more or less in the middle of the lateral surface of the developing scapula. Thus, the floor of the supraspinous fossa is present from the beginning of scapular development, simultaneously with the infraspinous fossa. The homology of the therian spine with the anterior border of the sauropsid and monotreme scapula is questioned. We consider the dorsal portion (as opposed to the ventral or acromial portion) of the scapular spine a neomorphic structure of therian mammals.

Animals↗
PubMed2003

Distribution of keratin and associated proteins in the epidermis of monotreme, marsupial, and placental mammals.

The expression of acidic and basic keratins, and of some keratinization marker proteins such as filaggrin, loricrin, involucrin, and trichohyalin, is known for the epidermis of only a few eutherian species. Using light and high-resolution immunocytochemistry, the presence of these proteins has been studied in two monotreme and five marsupial species and compared to that in eutherians. In both monotreme and marsupial epidermis lamellar bodies occur in the upper spinosus and granular layers. Development of the granular layer varies between species and regionally within species. There is great interspecific variation in the size (0.1-3.0 microm) of keratohyalin granules (KHGs) associated with production of orthokeratotic corneous tissues. Those skin regions lacking hairs (platypus web), or showing reduced pelage density (wombat) have, respectively, minute or indiscernible KHGs, associated with patchy, or total, parakeratosis. Ultrastructural analysis shows that monotreme and marsupial KHGs comprise irregular coarse filaments of 25-40 nm that contact keratin filaments. Except for parakeratotic tissues of platypus web, distribution of acidic and basic proteins in monotreme and marsupial epidermis as revealed by anti-keratin antibodies AE1, AE2, and AE3 resembles that of eutherian epidermis. Antibodies against human or rat filaggrins have little or no cross-reactivity with epidermal proteins of other mammals: only sparse areas of wombat and rabbit epidermis show a weak immunofluorescence in transitional cells and in the deepest corneous tissues. Of the available, eutherian-derived antibodies, that against involucrin shows no cross-reactivity with any monotreme and marsupial epidermal tissues and that against trichohyalin cross-reacts only with cells in the inner root sheath and medulla of hairs. These results suggest that if involucrin and trichohyalin are present throughout noneutherian epidermis, they may have species-specific molecular structures. By contrast, eutherian-derived anti-loricrin antibodies show a weak to intense cross-reactivity to KHGs and corneous tissues of both orthokeratotic and parakeratotic epidermis in monotremes and marsupials. High-resolution immunogold analysis of loricrin distribution in immature keratinocytes of platypus parakeratotic web epidermis identifies labeled areas of round or irregular, electron-pale granules within the denser keratohyalin component and keratin network. In the deepest mature tissues, loricrin-like labeling is diffuse throughout the cytoplasm, so that cells lack the preferential distribution of loricrin along the corneous envelope that characterizes mature eutherian keratinocytes. Thus, the irregular distribution of loricrin in platypus parakeratotic tissues more resembles that which has been described for reptilian and avian keratinocytes. These observations on the noneutherian epidermis show that a stratum granulosum is present to different degrees, even discontinuous within one tissue, so that parakeratotic and orthokeratotic areas may alternate: this might imply that parakeratotic monotreme epidermis reflects the primitive pattern of amniote alpha-keratogenesis. Absent from anamniote epidermis and all sauropsid beta-keratogenic tissues, the ubiquitous presence of a loricrin-like protein as a major component of other amniote corneous tissues suggests that this is a primitive feature of amniote alpha-keratogenesis. The apparent lack of specific regionalization of loricin near the plasma membranes of monotreme keratinocytes could be an artifactual result of the immunofluorescence technique employed, or there may be masking of the antigenicity of loricrin-like proteins once they are incorporated into the corneous envelope. Nevertheless, the mechanism of redistribution of such proteins during maturation of monotreme keratinocytes is different from, perhaps more primitive, or less specialized, than that in the epidermis of eutherian mammals.

Animals↗
PubMed2004

Fine structure of marsupial hairs, with emphasis on trichohyalin and the structure of the inner root sheath.

The fine structure and cornification of marsupial hairs are unknown. The distribution of keratins, trichohyalin, and transglutaminase in marsupial hairs was studied here for the first time by electron microscopy and immunocytochemistry. The localization of acidic and basic keratins in marsupial hairs is similar to that of hairs in placental mammals, and the keratins are mainly localized in the outer root sheath and surrounding epidermis. Marsupial trichohyalin in both medulla and inner root sheath (IRS) cross-reacts with a trichohyalin antibody that recognizes trichohyalin across placental species, indicating a common epitope(s) among mammalian trichohyalin. Roundish to irregular trichohyalin granules are composed of a network of immunolabeled 10-15-nm-thick coarse filaments within an amorphous matrix in which a weak labeling for transglutaminases is present. This suggests that the enzyme, and its substrate trichohyalin, are associated in mature granules. Transglutaminase labeling mainly occurs in condensing chromatin of mature cells of the outer and inner root sheaths, suggesting formation of the nuclear envelope connected with terminal differentiation of these cells. In mature Huxley or Henle layers the filaments lose the immunolabeling for trichohyalin when they are reoriented into parallel rows linked by short bridges, thus suggesting that the filaments with their reactive epitopes are chemically modified during cornification, as seen in the IRS of hairs of placental mammals. The Huxley layer probably acts as a cushion, absorbing the tensions connected with the distalward movement of the growing hair fiber. Variations in stratification of the Huxley layer are probably related to the diameter of the hair shaft. The cytoplasmic and junctional connections between cells of the Huxley layer and the companion layer and the outer root sheath enhance the grip of the IRS and hair fiber within the follicle. The role of cells of the IRS in sculpturing the fiber cuticle and in the mechanism of shedding that allows the exit of hair on the epidermal surface in mammals are discussed.

Animals↗
PubMed2006

Evidence at hand: Diversity, functional implications, and locomotor prediction in intrinsic hand proportions of diprotodontian marsupials.

Knowledge about the diversity, locomotor adaptations, and evolution of the marsupial forelimb is limited, resulting in an underrepresentation of marsupials in comparative anatomical literature on mammalian forelimb anatomy. This study investigated hand proportions in the diverse marsupial order Diprotodontia. Fifty-two measurements of 95 specimens representing 47 species, as well as 6 non-diprotodontian specimens, were explored using principal components analysis (PCA). Bootstrapping was used to assess the reliability of the loadings. Phylogenetically independent contrasts and phylogenetic ANOVA were used to test for correlation with size and functional adaptation of forelimbs for locomotor habit, scored as arboreal vs. terrestrial. Analysis of first principal component (PC1) scores revealed significant differences between arboreal and terrestrial species, and was related to relative slenderness of their phalangeal elements. Both locomotor groups displayed allometry along PC1 scores, but with different intercepts such that PC1 discriminated between the two locomotor habits almost completely. PC2 separated some higher-level clades and burrowing species. Analysis of locomotor predictors commonly applied by palaeontologists indicates that ratios between proximal and intermediate phalanges were unsuitable as predictors of arboreality/terrestriality, but the phalangeal index was more effective. From PCA results, a phalangeal slenderness ratio was developed which proved to be a useful discriminator, suggesting that a single unallocated phalanx can be used for an impression of locomotor mode in fossils. Most Diprotodontia are laterally paraxonic or ectaxonic, with the exception of digging species whose hands are medially paraxonic. Our results complement those of studies on placental mammals, suggesting that the demands of arboreality, terrestriality, or frequent digging on intrinsic hand proportions are met with similar anatomical adaptations in marsupials.

Adaptation, Physiological↗
PubMed1977

Oxytalan fibre organization in marsupial mandibular periodontal tissues.

The arrangement and distribution of oxytalan fibres in Australian marsupials has not previously been reported. Periodontal tissues of wombat, wallaby, possum, and marsupial mouse were examined to ascertain oxytalan fibre organization. Despite adaptation of the marsupial masticatory apparatus to different diets the oxytalan fibre organization in the periodontal ligament shows a basic pattern which corresponds with that reported in other animals. The oxytalan system forms a continuous meshwork of fine, branching fibres which completely invests each tooth root and connects adjacent teeth. Thick ribbon-like apico-occlusally orientated oxytalan fibres, thought to form by the coalescence of thinner fibres, are restricted to the periodontal ligament. The oxytalan fibres are embedded in cementum and attached to blood vessels in the pariodontal ligament. Oxytalan fibres do not insert into alveolar bone. Histological evidence indicates functional remodelling of the oxytalan fibre system in continuously erupting teeth.

Animals↗
PubMed1983

Cleavage in vivo and in culture in the Dasyurid marsupial Antechinus stuartii (macleay).

Cleavage in the brown marsupial mouse, Antechinus stuartii, from the zygote to the unilaminar blastocyst, was observed in vivo and in culture and in sections of embryos. The first three divisions were meridional and passed from the yolk pole to the opposite pole. Deutoplasmolysis, resulting in a distinct yolk mass, occurred during the first two divisions. Prior to the third and fourth divisions, the blastomeres elongated and flattened against the zona pellucida. The fourth division was latitudinal and resulted in two histologically distinct rings of eight blastomeres which were at first rounded and then became flattened against the zona. Further divisions and flattening of the blastomeres resulted in a complete unilaminar blastocyst by the time the blastocyst numbered 22 to 30 cells. Some expansion, causing compression of the zona and mucoid layers, occurred before completion of the blastocyst, but most expansion occurred once the blastocyst was complete. No histological differences could be detected between the blastomeres at this stage. Embryos were successfully cultured from the zygote to the rounded four-cell stage and from the flattened four-cell stage to the completed unilaminar blastocyst of around 32 cells. Total estimated cleavage times were slower in culture than in vivo, but the relative lengths of time for each division were approximately the same.

Animals↗
PubMed1985

Use of the term "trophoblast" for tissues in therian mammals.

Use of the term "trophoblast" in descriptions of therian (marsupial and eutherian) mammals has caused confusion because of misinterpretations of blastular homologies and because of imprecise application in functional versus ontogenetic-phylogenetic senses. Marsupials follow the plan of early development characteristic of noneutherian amniotes. Eutherians, in contrast, are unique in the early determination of presumptive embryonic versus extraembryonic cells through formation of inner cell mass versus trophoblastic (or trophectodermal) tissues, respectively. No cellular unit of the eutherian blastula is recognizable unequivocally as the homologue of a specific part of the protodermal marsupial blastula; progressive deletion of innovative but phylogenetically older ontogenetic steps probably figured importantly in the evolution of eutherian early embryogenesis. Because of marked differences in mode of formation and in cellular fates, homology of the blastocoel between marsupials and eutherians is questioned. It is suggested that use of the term "trophoblast" be restricted to eutherians in discussions of ontogenesis or phylogenesis, and be deemphasized in the functional sense (i.e., fetal-maternal exchanges) for marsupials, in favor of the more appropriate tissue terms of "choriovitelline" and "chorioallantoic" membranes. Integral to the origin of the eutherian style of embryogenesis was the evolution during Cretaceous time of neomorphic, extraembryonic tissues (i.e., trophoblast) having physiological properties that allowed the unique combination of intimate apposition of fetal and maternal tissues and circulatory systems, along with sustained, active morphogenesis. Marsupials have not achieved such a combination.

Animals↗
PubMed1988

Trophoblast concept as applied to therian mammals.

Available evidence provides little support for a recent proposal that the term "trophoblast" be applied solely to eutherian mammals. Arguments for such a restricted usage are based on a dichotomous interpretation of therian reproduction that underestimates the developmental, structural, and functional diversity of trophoblastic tissues occurring within the infraclass Eutherian. The occurrence of developmental patterns that are phenotypically intermediate between those of commonly studied eutherians and metatherians suggests that blastocyst development is not fundamentally different in marsupials and eutherians. The trophoblast of marsupials accomplishes most or all of the major functions of the eutherian trophoblast, including maternal-fetal physiological exchange, implantation, contribution to placental membranes, steroid metabolism, and possibly, immunological protection of the conceptus. Furthermore, application of the term "trophoblast" to marsupials is consistent with present and past usage, as well as with the original definition and etymological derivation of the term. Therefore, we recommend that the term "trophoblast" continue to be applied in a functional-morphological sense to the appropriate extraembryonic tissues of marsupials. Such use of functional (rather than taxonomic) criteria for application of this term avoids biasing interpretations of mammalian reproductive evolution.

Animals↗
PubMed1990

Morphological changes in the oocyte and its surrounding vestments during in vivo fertilization in the dasyurid marsupial Sminthopsis crassicaudata.

This light and transmission electron microscopical study shows that the first polar body is given off before ovulation and that part of its cell membrane and that of the surrounding oocyte have long microvilli at the time of its ejection. Several layers of cumulus cells initially surround the secondary oocyte and first polar body, but the ovulated oocytes in the oviducts in the process of being fertilized do not have cumulus cells around them. Partly expelled second polar bodies occur in the oviduct; they are elongated structures that lack organelles and have electron-dense nuclei. A small fertilization cone appears to form around the sperm tail at the time of sperm entry into the egg and an incorporation cone develops around the sperm head in the egg cytoplasm. In three fertilized eggs a small hole was seen in the zona, which was presumably formed by the spermatozoon during penetration. Cortical granules, present in ovarian oocytes, are not seen in fertilized tubal or uterine eggs; release of their contents probably reduces the chances of polyspermy, although at least one polyspermic fertilized egg was seen and several other fertilized eggs had spermatozoa within the zona pellucida. In the zygote the pronuclei come to lie close together, but there was no evidence of fusion. A "yolk mass," which becomes eccentric before ovulation, is extruded by the time the two-cell embryos are formed, but many vacuoles remain in the non-yolky pole of the egg. A shell membrane of variable thickness is present around all uterine eggs but its origin remains undetermined.

Animals↗