Limits...
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.


Scheme of bud development in T. wilhelma. (A) Four bud stages are characteristic, with the first three connected to the mother sponge by a stalk: Skeletal elements in red (megasclere bundles and aster spheres); megasclere bundles partly simplified as cylinders; Tissue in grey, separated into cortex (light grey) and choanoderm (dark grey). (B) Details of bud stages (left) and schematic graphs of morphological functional unit distribution. There are indications of rotational symmetry along the initial connecting stalk (st) in stages one to three (compare Additional file 4). Stage 4 buds display an adult-like body morphology with point symmetry to the skeleton centre (sc; see Additional file 5). Choanoderm development starts in stage 2, accompanied by the development of the megaster spheres in stage 3. Differentiation into a cortex (co) and choanoderm (cd) is characterized by the development of the aquiferous system (larger canals in stage 2; lacunae in stage 3). Body extensions (ext) (filaments) are found in stage 4 buds. For further details see text.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2749020&req=5

Figure 6: Scheme of bud development in T. wilhelma. (A) Four bud stages are characteristic, with the first three connected to the mother sponge by a stalk: Skeletal elements in red (megasclere bundles and aster spheres); megasclere bundles partly simplified as cylinders; Tissue in grey, separated into cortex (light grey) and choanoderm (dark grey). (B) Details of bud stages (left) and schematic graphs of morphological functional unit distribution. There are indications of rotational symmetry along the initial connecting stalk (st) in stages one to three (compare Additional file 4). Stage 4 buds display an adult-like body morphology with point symmetry to the skeleton centre (sc; see Additional file 5). Choanoderm development starts in stage 2, accompanied by the development of the megaster spheres in stage 3. Differentiation into a cortex (co) and choanoderm (cd) is characterized by the development of the aquiferous system (larger canals in stage 2; lacunae in stage 3). Body extensions (ext) (filaments) are found in stage 4 buds. For further details see text.

Mentions: Assuming development is continuous, the distinct stages in bud development in T. wilhelma represent important milestones of bud morphogenesis. The morphological changes are schematically summarized in Figure 6. Budding starts with the migration of cells and the transportation of the first megascleres into the early bud [not investigated here, for details see [31]]. Stage 1 buds are dominated by the stalk connecting the bud and the mother sponge, which also represents a first symmetry axis (Fig. 6B1, see Additional file 4). Cells migrating into the emerging bud from the mother sponge arrange axisymmetrically around the tip of the stalk, forming a characteristic small bulb. The future skeletal centre is formed within the centre of this cellular bulb (Fig. 6B2). The overall spatiotemporal pattern of bud morphological development is characterized by several temporally overlapping processes: 1. Rearrangement of megascleres from the primary axis via a planar star to a spherical star shape. 2. Formation of the aquiferous system, constituted by choanocyte chamber differentiation (compare Fig. 1) and canal formation. 3. Differentiation of a choanosomal centre and a cortical region, which seems not to start before the skeleton merges from the planar star to the spherical star shape (Fig. 6B3-4; compare Figs. 3B-C and see Additional file 3B-C). This process coincides in most cases with the release from the mother sponge, and we regard it as the onset of the full functionality of the aquiferous system. A comparison between bud sizes and the proportion of skeletal elements to tissue reveals no correlation (see Additional file 2), so bud size does not seem to be significant in the spatiotemporal pattern of bud development.


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)

Scheme of bud development in T. wilhelma. (A) Four bud stages are characteristic, with the first three connected to the mother sponge by a stalk: Skeletal elements in red (megasclere bundles and aster spheres); megasclere bundles partly simplified as cylinders; Tissue in grey, separated into cortex (light grey) and choanoderm (dark grey). (B) Details of bud stages (left) and schematic graphs of morphological functional unit distribution. There are indications of rotational symmetry along the initial connecting stalk (st) in stages one to three (compare Additional file 4). Stage 4 buds display an adult-like body morphology with point symmetry to the skeleton centre (sc; see Additional file 5). Choanoderm development starts in stage 2, accompanied by the development of the megaster spheres in stage 3. Differentiation into a cortex (co) and choanoderm (cd) is characterized by the development of the aquiferous system (larger canals in stage 2; lacunae in stage 3). Body extensions (ext) (filaments) are found in stage 4 buds. For further details see text.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Scheme of bud development in T. wilhelma. (A) Four bud stages are characteristic, with the first three connected to the mother sponge by a stalk: Skeletal elements in red (megasclere bundles and aster spheres); megasclere bundles partly simplified as cylinders; Tissue in grey, separated into cortex (light grey) and choanoderm (dark grey). (B) Details of bud stages (left) and schematic graphs of morphological functional unit distribution. There are indications of rotational symmetry along the initial connecting stalk (st) in stages one to three (compare Additional file 4). Stage 4 buds display an adult-like body morphology with point symmetry to the skeleton centre (sc; see Additional file 5). Choanoderm development starts in stage 2, accompanied by the development of the megaster spheres in stage 3. Differentiation into a cortex (co) and choanoderm (cd) is characterized by the development of the aquiferous system (larger canals in stage 2; lacunae in stage 3). Body extensions (ext) (filaments) are found in stage 4 buds. For further details see text.
Mentions: Assuming development is continuous, the distinct stages in bud development in T. wilhelma represent important milestones of bud morphogenesis. The morphological changes are schematically summarized in Figure 6. Budding starts with the migration of cells and the transportation of the first megascleres into the early bud [not investigated here, for details see [31]]. Stage 1 buds are dominated by the stalk connecting the bud and the mother sponge, which also represents a first symmetry axis (Fig. 6B1, see Additional file 4). Cells migrating into the emerging bud from the mother sponge arrange axisymmetrically around the tip of the stalk, forming a characteristic small bulb. The future skeletal centre is formed within the centre of this cellular bulb (Fig. 6B2). The overall spatiotemporal pattern of bud morphological development is characterized by several temporally overlapping processes: 1. Rearrangement of megascleres from the primary axis via a planar star to a spherical star shape. 2. Formation of the aquiferous system, constituted by choanocyte chamber differentiation (compare Fig. 1) and canal formation. 3. Differentiation of a choanosomal centre and a cortical region, which seems not to start before the skeleton merges from the planar star to the spherical star shape (Fig. 6B3-4; compare Figs. 3B-C and see Additional file 3B-C). This process coincides in most cases with the release from the mother sponge, and we regard it as the onset of the full functionality of the aquiferous system. A comparison between bud sizes and the proportion of skeletal elements to tissue reveals no correlation (see Additional file 2), so bud size does not seem to be significant in the spatiotemporal pattern of bud development.

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.