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ABSTRACT: Our current understanding of the lungfish immune system is limited. This study is characterizing the immune cells separated from primary and secondary immune organs of the Australian lungfish, Neoceratodus forsteri. Our functional studies utilized flow cytometry to study the immune cells extracted from the thymus, spiral valve intestine, spleen, and kidney. The different characteristics of lymphocytes and granulocytes were analyzed by utilization of viability, phagocytosis, oxidative burst, and apoptosis assays. Most of the nonviable intestinal cells were lymphocytes. Depending on the organ, 6-25% of the total population, predominantly granulocytes, underwent phagocytosis where the splenic cells were the most and intestinal cells the least phagocytic cells. Cells responded positively but differently to stimulation with phorbol myristate acetate (PMA) to produce radical oxygen species, an indication of their oxidative burst activity, which was mainly associated with granulocytes. Although cells were induced by dexamethasone to undergo apoptosis, such an induction did not follow a consistent pattern of dose of dexamethasone or incubation time between the different organs. In the absence of monoclonal antibodies against lungfish immune cells, these functional flow cytometric analyses aid our understanding on the functionality of immune cells.
Fish & Shellfish Immunology 04/2013; · 3.32 Impact Factor
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ABSTRACT: Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.
PLoS Biology 10/2011; 9(10):e1001168. · 11.45 Impact Factor
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ABSTRACT: We report a temporal order of tooth addition in the Australian lungfish where timing of tooth induction is
sequential in the same pattern as osteichthyans along the lower jaw. The order of tooth initiation in
Neoceratodus starts from the midline tooth, together with left and right ones at jaw position 2, followed by 3
and then 1. This is the pattern order for dentary teeth of several teleosts and what we propose represents a
stereotypic initiation pattern shared with all osteichthyans, including the living sister group to all tetrapods,
the Australian lungfish. This is contrary to previous opinions that the lungfish dentition is otherwise
derived and uniquely different. Sonic hedgehog (shh) expression is intensely focused on tooth positions at
different times corresponding with their initiation order. This deployment of shh is required for lungfish
tooth induction, as cyclopamine treatment results in complete loss of these teeth when applied before they
develop. The temporal sequence of tooth initiation is possibly regulated by shh and is know to be required
for dentition pattern in other osteichthyans, including cichlid fish and snakes. This reflects a shared
developmental process with jawed vertebrates at the level of the tooth module but differs with the lack of
replacement teeth.
Philosophical Transactions of The Royal Society B Biological Sciences 11/2009; 276:623-631. · 6.40 Impact Factor
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ABSTRACT: The vertebrate thymus consists of distinctive subpopulations of epithelial cells that contain a diverse repertoire of cytoskeletal proteins. In this study of the thymus in the Australian lungfish, Neoceratodus forsteri, immunohistochemistry was used to distinguish the cytoskeletal proteins present in each class of thymic epithelial cell. A panel of antibodies (Abs), each specific for a different cytoskeletal polypeptide (keratins, vimentin, desmin, actin and tubulins), was used on paraffin and ultrathin resin sections of thymus. Ab AE I (reactive against human type I cytokeratins (CK) 14, 16 and 19) selectively stained the cytoplasm of capsular, trabecular and the outermost epithelial cells of Hassall's corpuscles. Anti-CK 10 Abs strongly labelled the capsular epithelial cells and less than 20% of cortical and medullary epithelial cells. The anti-50-kDa desmin Ab did not react with any thymic cells, whereas the anti-53-kDa desmin Ab labelled some capsular, cortical and medullary thymic epithelial cells. The anti-vimentin Ab stained most of the capsular and ~60% of the cortical epithelium. Thymic nurse cells and Hassall's corpuscles were found to be devoid of actin, which was strongly detected in medullary and perivascular epithelium. Both alpha and beta tubulins were detected in all thymic cells. This study extends the concept of thymic epithelial heterogeneity. The complexity of thymic epithelium in N. forsteri may indicate a relationship between thymic epithelial subpopulations and the thymic microenvironment. These data identify anti-keratin Abs as a valuable tool for studying differentiation and ontogeny of the thymic epithelium in N. forsteri.
Journal of Anatomy 02/2009; 214(1):140-52. · 2.37 Impact Factor
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01/2009; 90:264-272.
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ABSTRACT: We report a temporal order of tooth addition in the Australian lungfish where timing of tooth induction is sequential in the same pattern as osteichthyans along the lower jaw. The order of tooth initiation in Neoceratodus starts from the midline tooth, together with left and right ones at jaw position 2, followed by 3 and then 1. This is the pattern order for dentary teeth of several teleosts and what we propose represents a stereotypic initiation pattern shared with all osteichthyans, including the living sister group to all tetrapods, the Australian lungfish. This is contrary to previous opinions that the lungfish dentition is otherwise derived and uniquely different. Sonic hedgehog (shh) expression is intensely focused on tooth positions at different times corresponding with their initiation order. This deployment of shh is required for lungfish tooth induction, as cyclopamine treatment results in complete loss of these teeth when applied before they develop. The temporal sequence of tooth initiation is possibly regulated by shh and is know to be required for dentition pattern in other osteichthyans, including cichlid fish and snakes. This reflects a shared developmental process with jawed vertebrates at the level of the tooth module but differs with the lack of replacement teeth.
Proceedings of the Royal Society B: Biological Sciences 12/2008; 276(1657):623-31. · 5.41 Impact Factor
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ABSTRACT: The cranial neural crest has been shown to give rise to a diversity of cells and tissues, including cartilage, bone and connective tissue, in a variety of tetrapods and in the zebrafish. It has been claimed, however, that in the Australian lungfish these tissues are not derived from the cranial neural crest, and even that no migrating cranial neural crest cells exist in this species. We have earlier documented that cranial neural crest cells do migrate, although they emerge late, in the Australian lungfish. Here, we have used the lipophilic fluorescent dye, DiI, to label premigratory cranial neural crest cells and follow their fate until stage 43, when several cranial skeletal elements have started to differentiate. The timing and extent of their migration was investigated, and formation of mandibular, hyoid and branchial streams documented. Cranial neural crest was shown to contribute cells to several parts of the head skeleton, including the trabecula cranii and derivatives of the mandibular arch (e.g., Meckel's cartilage, quadrate), the hyoid arch (e.g., the ceratohyal) and the branchial arches (ceratobranchials I-IV), as well as to the connective tissue surrounding the myofibers in cranial muscles. We conclude that cranial neural crest migration and fate in the Australian lungfish follow the stereotyped pattern documented in other vertebrates.
Journal of Experimental Zoology Part B Molecular and Developmental Evolution 07/2008; 310(4):345-54. · 2.42 Impact Factor
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ABSTRACT: A defining feature of tetrapod evolutionary origins is the transition from fish fins to tetrapod limbs. A major change during this transition is the appearance of the autopod (hands, feet), which comprises two distinct regions, the wrist/ankle and the digits. When the autopod first appeared in Late Devonian fossil tetrapods, it was incomplete: digits evolved before the full complement of wrist/ankle bones. Early tetrapod wrists/ankles, including those with a full complement of bones, also show a sharp pattern discontinuity between proximal elements and distal elements. This suggests the presence of a discontinuity in the proximal-distal sequence of development. Such a discontinuity occurs in living urodeles, where digits form before completion of the wrist/ankle, implying developmental independence of the digits from wrist/ankle elements. We have observed comparable independent development of pectoral fin radials in the lungfish Neoceratodus (Osteichthyes: Sarcopterygii), relative to homologues of the tetrapod limb and proximal wrist elements in the main fin axis. Moreover, in the Neoceratodus fin, expression of Hoxd13 closely matches late expression patterns observed in the tetrapod autopod. This evidence suggests that Neoceratodus fin radials and tetrapod digits may be patterned by shared mechanisms distinct from those patterning the proximal fin/limb elements, and in that sense are homologous. The presence of independently developing radials in the distal part of the pectoral (and pelvic) fin may be a general feature of the Sarcopterygii.
Journal of Experimental Zoology Part B Molecular and Developmental Evolution 01/2008; 308(6):757-68. · 2.42 Impact Factor
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ABSTRACT: The enigmatic Devonian fossil Palaeospondylus gunni was identified as a larval form, metamorphosing into the lungfish Dipterus valenciennesi. Morphological features used to identify P. gunni as a larval lungfish include enlarged cranial ribs, rudimentary limb girdles, and absence of teeth. However, this combination of features does not characterize the extant lungfish Neoceratodus forsteri, even at very young stages, nor early stages of Devonian and younger fossil lungfish. Absence of teeth is problematic because early ontogenetic stages of fossil and living lungfish possess full dentitions including marginal teeth. Also problematic are cranial ribs as a defining character of lungfish, as these also occur in certain actinopterygians. It is argued that Neoceratodus is an obligate neotene (reproductively mature larva), with the implication that metamorphosis was a feature of the ontogeny of early lungfish. Pedomorphic characters have been recognized in Neoceratodus and other post-Devonian lungfish, including large cells and correspondingly large genome size; these latter characters correlate with neoteny in salamanders. Small cells preserved in fossil bone suggest that Devonian lungfish had a smaller genome than post-Devonian lungfish, implying that they were not neotenic. As fossil lungfish cell sizes (and genomes) increased in the late Paleozoic, the diversity of lungfish morphologies decreased, so that taxa like Sagenodus and Conchopoma show morphological similarity to Neoceratodus, marking a point in phylogeny at which metamorphosis was potentially lost. Since ancestral larval characters are retained in neotenic adults, we predict that Devonian larvae should resemble these post-Devonian taxa, a prediction which Palaeospondylus does not fulfill.
Journal of Experimental Zoology Part B Molecular and Developmental Evolution 04/2007; 308(2):163-71. · 2.42 Impact Factor
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Journal of Experimental Zoology Part B-molecular and Developmental Evolution - J EXP ZOOL PART B. 01/2007;
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ABSTRACT: Differentiation of the axial skeleton into distinct regions, once thought to be characteristic of the Tetrapoda, also occurs in the actinopterygian Danio rerio. In these taxa, the boundary between the cervical-thoracic regions correlates with Hoxc6 expression and morphological features such as position of the pectoral fin and associated nerves, and the absence of ribs. In the lungfish Neoceratodus, a member of the extant sister taxon to the Tetrapoda, the first vertebral element to chondrify is situated well posterior to the skull, developing from somites 6 and 7 (6/7) and associated with an enlarged cranial rib and nerves innervating the pectoral fin. Two vertebral elements develop later and more anteriorly, associated with somites 4/5 and 5/6. These three elements become incorporated into the occipital region of the skull during Neoceratodus ontogeny, until the cranial rib itself articulates to the rear of the skull. These features of early development indicate a regionalization of the Neoceratodus vertebral column: the cranial rib marks the boundary between the cervical and thoracic regions, the two more anterior vertebrae lacking ribs represent the cervical region, while somites 1-4 (cranial half), lacking any vertebral development, represent the occipital region. However, the cervical region of the vertebral column is effectively lost during ontogeny of Neoceratodus. A recognizable cervical region in the tetrapod vertebral column, as in zebrafish, suggests that cervical vertebrae are not incorporated into the skull but maintained as distinct elements of the column, representing an important shift in relative developmental timing and the influence of heterochrony in this region during the fish-tetrapod transition.
Journal of Experimental Zoology Part B Molecular and Developmental Evolution 06/2005; 304(3):229-37. · 2.42 Impact Factor
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ABSTRACT: The development of the nervus terminalis system in the lungfish, Neoceratodus forsteri, was investigated by using FMRFamide as a marker. FMRFamide immunoreactivity appears first within the brain, in the dorsal hypothalamus at a stage around hatching. At a slightly later stage, immunoreactivity appears in the olfactory mucosa. These immunoreactive cells move outside the olfactory organ to form the ganglion of the nervus terminalis. Immunoreactive processes emerge from the ganglion of the nervus terminalis in two directions, one which joins the olfactory nerve to travel to the brain and the other which courses below the brain to enter at the level of the preoptic nucleus. Neither the ganglion of the nervus terminalis nor the two branches of the nervus terminalis form after surgical removal of the olfactory placode at a stage before the development of FMRFamide immunoreactivity external to the brain. Because this study has confirmed that the nervus terminalis in lungfish comprises both an anterior and a posterior branch, it forms the basis for discussion of homology between these branches and the nervus terminalis of other anamniote vertebrates.
The Journal of Comparative Neurology 09/2002; 450(2):115-21. · 3.81 Impact Factor
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ABSTRACT: The lungfish dentition is different from other osteichthyan fish because it has a characteristic and unique pattern of teeth arranged as toothplates. Growth, addition of teeth, and retention as part of a statodont dentition are determined by the initiation pattern. In adult lungfish new teeth are only added laterally to each radial row in the dentition. This is in marked contrast to marginal rows of teeth with regular, alternating replacement in most osteichthyans. We analyze development from fossil hatchling forms of the Late Devonian dipnoan Andreyevichthys and compare with those of Neoceratodus, the Australian lungfish. The specific pattern of development, unique within lungfish, is also present in the transitory, marginal, anterior dentition in both, reflecting a strongly conserved developmental pattern. These marginal teeth form but are then lost in both, so that also this program of development is conserved within lungfish for 360 million years, from the earliest known form.
Connective Tissue Research 02/2002; 43(2-3):113-9. · 1.20 Impact Factor
