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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).

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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).

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3D volume renderings of stage 1 to 4 buds of T. wilhelma and corresponding virtual sections from SR-μCT data elucidating the development of distinct morphological structures. (A) stage 1 bud without choanoderm/cortex differentiation (msb - megasclere bundle); (B) stage 2 bud without a separated choanoderm (dcd - developing choanoderm, dco - developing cortex) 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, the latter displaying lacunar cavities.
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Figure 4: 3D volume renderings of stage 1 to 4 buds of T. wilhelma and corresponding virtual sections from SR-μCT data elucidating the development of distinct morphological structures. (A) stage 1 bud without choanoderm/cortex differentiation (msb - megasclere bundle); (B) stage 2 bud without a separated choanoderm (dcd - developing choanoderm, dco - developing cortex) 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, the latter displaying lacunar cavities.

Mentions: Stage 1 buds exhibit a homogenous distribution of tissue and aquiferous system components (Figs. 3A). Cortex and choanosome are not differentiated, neither are lacunar cavities and choanocyte chambers (Figs 3A, 4A, 5A, and see Additional file 3A). The proportional volume of the skeleton is almost constant at around 1.5% throughout the complete specimen. In the stalk that connects the bud with the mother sponge, however, the proportional skeletal volume increases to over 30% (see Additional file 3A, arrowhead). The megasclere bundle of the stalk defines the main axis of the bud skeleton and consequently the whole bud at this stage. The overall appearance of the bud at this stage is flat and elongated along its axis (Fig. 4A, see Additional file 4). Apart from the stalk, a few megasclere bundles start to form around the future centre of the skeleton. All the bundles are arranged in a plane perpendicular to the stalk (see Additional files 3A and 4).


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)

3D volume renderings of stage 1 to 4 buds of T. wilhelma and corresponding virtual sections from SR-μCT data elucidating the development of distinct morphological structures. (A) stage 1 bud without choanoderm/cortex differentiation (msb - megasclere bundle); (B) stage 2 bud without a separated choanoderm (dcd - developing choanoderm, dco - developing cortex) 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, the latter displaying lacunar cavities.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: 3D volume renderings of stage 1 to 4 buds of T. wilhelma and corresponding virtual sections from SR-μCT data elucidating the development of distinct morphological structures. (A) stage 1 bud without choanoderm/cortex differentiation (msb - megasclere bundle); (B) stage 2 bud without a separated choanoderm (dcd - developing choanoderm, dco - developing cortex) 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, the latter displaying lacunar cavities.
Mentions: Stage 1 buds exhibit a homogenous distribution of tissue and aquiferous system components (Figs. 3A). Cortex and choanosome are not differentiated, neither are lacunar cavities and choanocyte chambers (Figs 3A, 4A, 5A, and see Additional file 3A). The proportional volume of the skeleton is almost constant at around 1.5% throughout the complete specimen. In the stalk that connects the bud with the mother sponge, however, the proportional skeletal volume increases to over 30% (see Additional file 3A, arrowhead). The megasclere bundle of the stalk defines the main axis of the bud skeleton and consequently the whole bud at this stage. The overall appearance of the bud at this stage is flat and elongated along its axis (Fig. 4A, see Additional file 4). Apart from the stalk, a few megasclere bundles start to form around the future centre of the skeleton. All the bundles are arranged in a plane perpendicular to the stalk (see Additional files 3A and 4).

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.


Related in: MedlinePlus