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The embryonic development of the central American wandering spider Cupiennius salei.

Wolff C, Hilbrant M - Front. Zool. (2011)

Bottom Line: The imaging procedure also elucidates the encircling border between the cell-dense embryo hemisphere and the hemisphere with much lower cell density (a structure termed 'equator' in earlier studies).Our improved staging system of development in C. salei development should be of considerable value to future comparative studies of animal development.A dense germ disc is not evident during development in C. salei, but we show that the gastrulation process is similar to that in spider species that do have a dense germ disc.

View Article: PubMed Central - HTML - PubMed

Affiliation: Humboldt-Universität zu Berlin Institut für Biologie/Vergleichende Zoologie Philippstraße 13, 10115 Berlin, Germany. carsten.wolff@rz.hu-berlin.de.

ABSTRACT

Background: The spider Cupiennius salei (Keyserling 1877) has become an important study organism in evolutionary and developmental biology. However, the available staging system for its embryonic development is difficult to apply to modern studies, with strong bias towards the earliest developmental stages. Furthermore, important embryonic events are poorly understood. We address these problems, providing a new description of the embryonic development of C. salei. The paper also discusses various observations that will improve our understanding of spider development.

Results: Conspicuous developmental events were used to define numbered stages 1 to 21. Stages 1 to 9 follow the existing staging system for the spider Achaearanea tepidariorum, and stages 10 to 21 provide a high-resolution description of later development. Live-embryo imaging shows cell movements during the earliest formation of embryonic tissue in C. salei. The imaging procedure also elucidates the encircling border between the cell-dense embryo hemisphere and the hemisphere with much lower cell density (a structure termed 'equator' in earlier studies). This border results from subsurface migration of primordial mesendodermal cells from their invagination site at the blastopore. Furthermore, our detailed successive sequence shows: 1) early differentiation of the precheliceral neuroectoderm; 2) the morphogenetic process of inversion and 3) initial invaginations of the opisthosomal epithelium for the respiratory system.

Conclusions: Our improved staging system of development in C. salei development should be of considerable value to future comparative studies of animal development. A dense germ disc is not evident during development in C. salei, but we show that the gastrulation process is similar to that in spider species that do have a dense germ disc. In the opisthosoma, the order of appearance of precursor epithelial invaginations provides evidence for the non-homology of the tracheal and book lung respiratory systems.

No MeSH data available.


Related in: MedlinePlus

Stages 7 and 8 of C. salei. Sytox staining, a-g; SEM, h. All scale bars 200 μm. a-d, Stage 7, Germ band. a: Posterior view of the growth zone (GZ), a dense region that is continuous with the primary thickening (PT) in stage 6, Figure 3h. The dorsal field (DF) is extended to its maximum. b: Same egg as in a rotated by 90 degrees, such that the embryo is in lateral view. The embryonic tissue (early germ band) extends along the ventral curvature between the two arrows. Between the two white arrow heads is the equator, which is the sharp change in cell density that marks the border of migration of mesendodermal cells from the primary thickening. c: Postero-lateral view of an embryo that is slightly more developed than the one in a and b. d: Lateral view of the same embryo as shown in c. The embryonic tissue (early germ band) extends along the ventral curvature between the two white arrows. This region has more cells and a much higher density than the dorsal field (DF). The equator is no longer visible. e-h, Stage 8, Segmented germ band. e: Lateral view. Evident are all future prosomal segments: cheliceres (Ch), pedipalps (P) and four walking legs (white arrow heads). At the posterior end, the growth zone (GZ) exhibits a higher density of cells. f: Frontal view of the same embryo as in e. g: Slightly more advanced embryo than e. Anterior to the cheliceral segment (Ch) the precheliceral region (Pc) is separated by a clear margin from the surrounding extra-embryonic (mainly yolk) tissue. All prosomal segments (cheliceres, Ch; pedipalps, P; four walking legs, L1-L4) are distinct. h: Lateral view. An embryo comparable to e. Evident are the germ band (GB) and yolk (Y). The yolk is located in the regions labelled earlier as the dorsal field (DF) and the extra-embryonic (Ee) region.
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Figure 4: Stages 7 and 8 of C. salei. Sytox staining, a-g; SEM, h. All scale bars 200 μm. a-d, Stage 7, Germ band. a: Posterior view of the growth zone (GZ), a dense region that is continuous with the primary thickening (PT) in stage 6, Figure 3h. The dorsal field (DF) is extended to its maximum. b: Same egg as in a rotated by 90 degrees, such that the embryo is in lateral view. The embryonic tissue (early germ band) extends along the ventral curvature between the two arrows. Between the two white arrow heads is the equator, which is the sharp change in cell density that marks the border of migration of mesendodermal cells from the primary thickening. c: Postero-lateral view of an embryo that is slightly more developed than the one in a and b. d: Lateral view of the same embryo as shown in c. The embryonic tissue (early germ band) extends along the ventral curvature between the two white arrows. This region has more cells and a much higher density than the dorsal field (DF). The equator is no longer visible. e-h, Stage 8, Segmented germ band. e: Lateral view. Evident are all future prosomal segments: cheliceres (Ch), pedipalps (P) and four walking legs (white arrow heads). At the posterior end, the growth zone (GZ) exhibits a higher density of cells. f: Frontal view of the same embryo as in e. g: Slightly more advanced embryo than e. Anterior to the cheliceral segment (Ch) the precheliceral region (Pc) is separated by a clear margin from the surrounding extra-embryonic (mainly yolk) tissue. All prosomal segments (cheliceres, Ch; pedipalps, P; four walking legs, L1-L4) are distinct. h: Lateral view. An embryo comparable to e. Evident are the germ band (GB) and yolk (Y). The yolk is located in the regions labelled earlier as the dorsal field (DF) and the extra-embryonic (Ee) region.

Mentions: The embryo now has two dissimilar egg hemispheres. The embryonic hemisphere appears to be more opaque because of the new layer of cells (primordial mesendoderm) underneath the ectoderm. The more translucent hemisphere is made up of extra-embryonic tissue, mainly filled with yolk in this and subsequent figures (e.g., Figures 3, 4, 5 and 6). The transition between the subsurface cell layer and the more translucent hemisphere has been called the 'equator' [26], and is clearly visible in living eggs (Figure 3e; Additional file 2). The cumulus is embedded at the edge of the equator and marks the anterior and dorsal region of the embryo body, while the primary thickening (in the centre of the embryonic hemisphere) is at the ventral and caudal pole of the embryo body (Figure 3e).


The embryonic development of the central American wandering spider Cupiennius salei.

Wolff C, Hilbrant M - Front. Zool. (2011)

Stages 7 and 8 of C. salei. Sytox staining, a-g; SEM, h. All scale bars 200 μm. a-d, Stage 7, Germ band. a: Posterior view of the growth zone (GZ), a dense region that is continuous with the primary thickening (PT) in stage 6, Figure 3h. The dorsal field (DF) is extended to its maximum. b: Same egg as in a rotated by 90 degrees, such that the embryo is in lateral view. The embryonic tissue (early germ band) extends along the ventral curvature between the two arrows. Between the two white arrow heads is the equator, which is the sharp change in cell density that marks the border of migration of mesendodermal cells from the primary thickening. c: Postero-lateral view of an embryo that is slightly more developed than the one in a and b. d: Lateral view of the same embryo as shown in c. The embryonic tissue (early germ band) extends along the ventral curvature between the two white arrows. This region has more cells and a much higher density than the dorsal field (DF). The equator is no longer visible. e-h, Stage 8, Segmented germ band. e: Lateral view. Evident are all future prosomal segments: cheliceres (Ch), pedipalps (P) and four walking legs (white arrow heads). At the posterior end, the growth zone (GZ) exhibits a higher density of cells. f: Frontal view of the same embryo as in e. g: Slightly more advanced embryo than e. Anterior to the cheliceral segment (Ch) the precheliceral region (Pc) is separated by a clear margin from the surrounding extra-embryonic (mainly yolk) tissue. All prosomal segments (cheliceres, Ch; pedipalps, P; four walking legs, L1-L4) are distinct. h: Lateral view. An embryo comparable to e. Evident are the germ band (GB) and yolk (Y). The yolk is located in the regions labelled earlier as the dorsal field (DF) and the extra-embryonic (Ee) region.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 4: Stages 7 and 8 of C. salei. Sytox staining, a-g; SEM, h. All scale bars 200 μm. a-d, Stage 7, Germ band. a: Posterior view of the growth zone (GZ), a dense region that is continuous with the primary thickening (PT) in stage 6, Figure 3h. The dorsal field (DF) is extended to its maximum. b: Same egg as in a rotated by 90 degrees, such that the embryo is in lateral view. The embryonic tissue (early germ band) extends along the ventral curvature between the two arrows. Between the two white arrow heads is the equator, which is the sharp change in cell density that marks the border of migration of mesendodermal cells from the primary thickening. c: Postero-lateral view of an embryo that is slightly more developed than the one in a and b. d: Lateral view of the same embryo as shown in c. The embryonic tissue (early germ band) extends along the ventral curvature between the two white arrows. This region has more cells and a much higher density than the dorsal field (DF). The equator is no longer visible. e-h, Stage 8, Segmented germ band. e: Lateral view. Evident are all future prosomal segments: cheliceres (Ch), pedipalps (P) and four walking legs (white arrow heads). At the posterior end, the growth zone (GZ) exhibits a higher density of cells. f: Frontal view of the same embryo as in e. g: Slightly more advanced embryo than e. Anterior to the cheliceral segment (Ch) the precheliceral region (Pc) is separated by a clear margin from the surrounding extra-embryonic (mainly yolk) tissue. All prosomal segments (cheliceres, Ch; pedipalps, P; four walking legs, L1-L4) are distinct. h: Lateral view. An embryo comparable to e. Evident are the germ band (GB) and yolk (Y). The yolk is located in the regions labelled earlier as the dorsal field (DF) and the extra-embryonic (Ee) region.
Mentions: The embryo now has two dissimilar egg hemispheres. The embryonic hemisphere appears to be more opaque because of the new layer of cells (primordial mesendoderm) underneath the ectoderm. The more translucent hemisphere is made up of extra-embryonic tissue, mainly filled with yolk in this and subsequent figures (e.g., Figures 3, 4, 5 and 6). The transition between the subsurface cell layer and the more translucent hemisphere has been called the 'equator' [26], and is clearly visible in living eggs (Figure 3e; Additional file 2). The cumulus is embedded at the edge of the equator and marks the anterior and dorsal region of the embryo body, while the primary thickening (in the centre of the embryonic hemisphere) is at the ventral and caudal pole of the embryo body (Figure 3e).

Bottom Line: The imaging procedure also elucidates the encircling border between the cell-dense embryo hemisphere and the hemisphere with much lower cell density (a structure termed 'equator' in earlier studies).Our improved staging system of development in C. salei development should be of considerable value to future comparative studies of animal development.A dense germ disc is not evident during development in C. salei, but we show that the gastrulation process is similar to that in spider species that do have a dense germ disc.

View Article: PubMed Central - HTML - PubMed

Affiliation: Humboldt-Universität zu Berlin Institut für Biologie/Vergleichende Zoologie Philippstraße 13, 10115 Berlin, Germany. carsten.wolff@rz.hu-berlin.de.

ABSTRACT

Background: The spider Cupiennius salei (Keyserling 1877) has become an important study organism in evolutionary and developmental biology. However, the available staging system for its embryonic development is difficult to apply to modern studies, with strong bias towards the earliest developmental stages. Furthermore, important embryonic events are poorly understood. We address these problems, providing a new description of the embryonic development of C. salei. The paper also discusses various observations that will improve our understanding of spider development.

Results: Conspicuous developmental events were used to define numbered stages 1 to 21. Stages 1 to 9 follow the existing staging system for the spider Achaearanea tepidariorum, and stages 10 to 21 provide a high-resolution description of later development. Live-embryo imaging shows cell movements during the earliest formation of embryonic tissue in C. salei. The imaging procedure also elucidates the encircling border between the cell-dense embryo hemisphere and the hemisphere with much lower cell density (a structure termed 'equator' in earlier studies). This border results from subsurface migration of primordial mesendodermal cells from their invagination site at the blastopore. Furthermore, our detailed successive sequence shows: 1) early differentiation of the precheliceral neuroectoderm; 2) the morphogenetic process of inversion and 3) initial invaginations of the opisthosomal epithelium for the respiratory system.

Conclusions: Our improved staging system of development in C. salei development should be of considerable value to future comparative studies of animal development. A dense germ disc is not evident during development in C. salei, but we show that the gastrulation process is similar to that in spider species that do have a dense germ disc. In the opisthosoma, the order of appearance of precursor epithelial invaginations provides evidence for the non-homology of the tracheal and book lung respiratory systems.

No MeSH data available.


Related in: MedlinePlus