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Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma.

Hammel JU, Herzen J, Beckmann F, Nickel M - Front. Zool. (2009)

Bottom Line: Based on morphometric data we defined four typical bud stages.Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed.Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität Jena, Erbertstr, 1, 07743 Jena, Germany. m.nickel@uni-jena.de.

ABSTRACT

Background: Primary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding.

Results: We investigated the budding process in Tethya wilhelma (Demospongiae) by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-muCT) image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens.

Conclusion: Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

No MeSH data available.


Volume analysis of body structures in T. wilhelma buds based on SR-μCT. (A) stage 1 bud without choanoderm/cortex differentiation; (B) stage 2 bud without a separated choanoderm but displaying the first differentiated aquiferous system canals; (C) stage 3 bud with an early developing choanoderm (dcd) and developing cortex (dco), (D - E) stage 4 buds with differentiated choanoderm (cd) and cortex (co) regions. Graphs represent relative volumetric proportions of all main morphological sponge structures: tissue (top row), aquiferous system (middle row) and skeleton (bottom row). Graph patterns typical for distinctly developed sponge regions are marked (sc - skeleton centre, ext - body extension (filaments), st - stalk). Volumetric results are given for the three main axes of the 3D data sets: x-axis (dashed), y-axis (dotted) and z-axis (solid).
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Figure 3: Volume analysis of body structures in T. wilhelma buds based on SR-μCT. (A) stage 1 bud without choanoderm/cortex differentiation; (B) stage 2 bud without a separated choanoderm but displaying the first differentiated aquiferous system canals; (C) stage 3 bud with an early developing choanoderm (dcd) and developing cortex (dco), (D - E) stage 4 buds with differentiated choanoderm (cd) and cortex (co) regions. Graphs represent relative volumetric proportions of all main morphological sponge structures: tissue (top row), aquiferous system (middle row) and skeleton (bottom row). Graph patterns typical for distinctly developed sponge regions are marked (sc - skeleton centre, ext - body extension (filaments), st - stalk). Volumetric results are given for the three main axes of the 3D data sets: x-axis (dashed), y-axis (dotted) and z-axis (solid).

Mentions: The graphs for each bud reveal characteristic spatiotemporal changes in the proportional volumes and quantitative distribution of canals, tissue and skeleton within the buds (Fig. 3). The overall graph shape for each structure changes specifically during bud formation and maturation and displays characteristic features at each stage. Newly formed buds display a homogenous distribution of tissue and aquiferous system elements (Fig. 3A). Step by step, the morphology changes into the adult phenotype, which is characterized by a high proportion of tissue in the sponge centre (the choanosome) and a high proportion of peripheral aquiferous system lacunae (the cortex), and by mineral scleres in the filamentous body extensions protruding from the sponge surface. As shown above, in juveniles which are fully functionally developed (late bud stages), all structures are represented by distinct peaks or plateaus. However, the cortex and choanosome also leave an imprint on the graphs in their early developmental stages (Fig. 3B-C).


Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma.

Hammel JU, Herzen J, Beckmann F, Nickel M - Front. Zool. (2009)

Volume analysis of body structures in T. wilhelma buds based on SR-μCT. (A) stage 1 bud without choanoderm/cortex differentiation; (B) stage 2 bud without a separated choanoderm but displaying the first differentiated aquiferous system canals; (C) stage 3 bud with an early developing choanoderm (dcd) and developing cortex (dco), (D - E) stage 4 buds with differentiated choanoderm (cd) and cortex (co) regions. Graphs represent relative volumetric proportions of all main morphological sponge structures: tissue (top row), aquiferous system (middle row) and skeleton (bottom row). Graph patterns typical for distinctly developed sponge regions are marked (sc - skeleton centre, ext - body extension (filaments), st - stalk). Volumetric results are given for the three main axes of the 3D data sets: x-axis (dashed), y-axis (dotted) and z-axis (solid).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2749020&req=5

Figure 3: Volume analysis of body structures in T. wilhelma buds based on SR-μCT. (A) stage 1 bud without choanoderm/cortex differentiation; (B) stage 2 bud without a separated choanoderm but displaying the first differentiated aquiferous system canals; (C) stage 3 bud with an early developing choanoderm (dcd) and developing cortex (dco), (D - E) stage 4 buds with differentiated choanoderm (cd) and cortex (co) regions. Graphs represent relative volumetric proportions of all main morphological sponge structures: tissue (top row), aquiferous system (middle row) and skeleton (bottom row). Graph patterns typical for distinctly developed sponge regions are marked (sc - skeleton centre, ext - body extension (filaments), st - stalk). Volumetric results are given for the three main axes of the 3D data sets: x-axis (dashed), y-axis (dotted) and z-axis (solid).
Mentions: The graphs for each bud reveal characteristic spatiotemporal changes in the proportional volumes and quantitative distribution of canals, tissue and skeleton within the buds (Fig. 3). The overall graph shape for each structure changes specifically during bud formation and maturation and displays characteristic features at each stage. Newly formed buds display a homogenous distribution of tissue and aquiferous system elements (Fig. 3A). Step by step, the morphology changes into the adult phenotype, which is characterized by a high proportion of tissue in the sponge centre (the choanosome) and a high proportion of peripheral aquiferous system lacunae (the cortex), and by mineral scleres in the filamentous body extensions protruding from the sponge surface. As shown above, in juveniles which are fully functionally developed (late bud stages), all structures are represented by distinct peaks or plateaus. However, the cortex and choanosome also leave an imprint on the graphs in their early developmental stages (Fig. 3B-C).

Bottom Line: Based on morphometric data we defined four typical bud stages.Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed.Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität Jena, Erbertstr, 1, 07743 Jena, Germany. m.nickel@uni-jena.de.

ABSTRACT

Background: Primary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding.

Results: We investigated the budding process in Tethya wilhelma (Demospongiae) by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-muCT) image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens.

Conclusion: Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

No MeSH data available.