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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

Stage 17, Dorsal closure. All scale bars 100 μm. Sytox staining, a-a''', c; SEMs, b, d, e. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared to previous stages (compare with Figure 12a). a': Frontal view. The white arrows indicate the direction of the epidermal and cuticular overgrowth of the brain region. a'': Posterior view. a''': Dorsal view. The white arrows indicate the dorsad growth of tissue that eventually forms the heart (H). b: Dorso-lateral view showing the crumbled appearance of the dorsal tissue directly posterior to the head lobes after dorsal closure. The prosomal tergites continue to extend dorsally (white arrows) (compare with Figure 12a). c: Detail of anterior prosoma. As a result of the forward positioning of the cheliceres and/or posterior positioning of the stomodeum, the labrum (Lb) is now between the bases of the cheliceres (Ch). Cuticular formations (white arrows) are visible in the sternal regions (white asterisks) of the prosomal segments. d: The right limb bud on opisthosomal segment two (O2) shows four pulmonary furrows (black arrows) and a lateral opening of the pulmonary sac (PuS). At the latero-posterior insertion of the limb bud at opisthosomal segment three (O3), the opening of the tubular trachea (TrO) is visible. e: Posterior opisthosomal region. The anlagen of the left and right tergite plates (Ter) meet dorso-medially (compare with a later stage, Figure 14c). en, endite; L1-L4, walking legs one to four; P, pedipalp; VS, ventral sulcus.
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Figure 13: Stage 17, Dorsal closure. All scale bars 100 μm. Sytox staining, a-a''', c; SEMs, b, d, e. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared to previous stages (compare with Figure 12a). a': Frontal view. The white arrows indicate the direction of the epidermal and cuticular overgrowth of the brain region. a'': Posterior view. a''': Dorsal view. The white arrows indicate the dorsad growth of tissue that eventually forms the heart (H). b: Dorso-lateral view showing the crumbled appearance of the dorsal tissue directly posterior to the head lobes after dorsal closure. The prosomal tergites continue to extend dorsally (white arrows) (compare with Figure 12a). c: Detail of anterior prosoma. As a result of the forward positioning of the cheliceres and/or posterior positioning of the stomodeum, the labrum (Lb) is now between the bases of the cheliceres (Ch). Cuticular formations (white arrows) are visible in the sternal regions (white asterisks) of the prosomal segments. d: The right limb bud on opisthosomal segment two (O2) shows four pulmonary furrows (black arrows) and a lateral opening of the pulmonary sac (PuS). At the latero-posterior insertion of the limb bud at opisthosomal segment three (O3), the opening of the tubular trachea (TrO) is visible. e: Posterior opisthosomal region. The anlagen of the left and right tergite plates (Ter) meet dorso-medially (compare with a later stage, Figure 14c). en, endite; L1-L4, walking legs one to four; P, pedipalp; VS, ventral sulcus.

Mentions: Dorsal closure completes inversion. The tergites of both body halves meet along the dorsal midline, covering all of the dorsal yolk with embryonic tissue. This gradual event starts posteriorly with the tergites of the caudal region and progresses anteriorly. The laterally expanding tissue of the prosomal tergites meets the tissue posterior to the precheliceral lobes (white arrows; Figure 13b). During the process, the dorsal prosomal surface has a crumpled appearance (Figure 13b). Underneath the area where the tergite plates touch each other, tissue that eventually forms the heart becomes evident (Figure 13a'''). Cuticle covers the sternites in the prosoma (white arrows; Figures 13c) and the brain region is also overgrown by epidermal and cuticular formations (white arrow; Figure 13a'). The embryonic tissue anterior to the pedipalp has bent posteriorly, marking the start of the process in which the supraoesophageal area folds onto the suboesophageal area. As a result of the positioning of the cheliceres and stomodeum, the labrum is positioned between the bases of the cheliceres (Figures 13a'. c). The pedipalps and walking legs have further extended and meet each other medially in a zipper-like manner. The posterior sides of the limb buds on opisthosomal segment two have become concave (Figure 13d). Evident on each bud are four pulmonary furrows (Figure 13d; black arrows) and the opening of the pulmonary sack (Figure 13d; white arrow). The segments posterior to opisthosomal segment eight have become compressed, giving them a swollen appearance (Figure 13e).


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

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

Stage 17, Dorsal closure. All scale bars 100 μm. Sytox staining, a-a''', c; SEMs, b, d, e. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared to previous stages (compare with Figure 12a). a': Frontal view. The white arrows indicate the direction of the epidermal and cuticular overgrowth of the brain region. a'': Posterior view. a''': Dorsal view. The white arrows indicate the dorsad growth of tissue that eventually forms the heart (H). b: Dorso-lateral view showing the crumbled appearance of the dorsal tissue directly posterior to the head lobes after dorsal closure. The prosomal tergites continue to extend dorsally (white arrows) (compare with Figure 12a). c: Detail of anterior prosoma. As a result of the forward positioning of the cheliceres and/or posterior positioning of the stomodeum, the labrum (Lb) is now between the bases of the cheliceres (Ch). Cuticular formations (white arrows) are visible in the sternal regions (white asterisks) of the prosomal segments. d: The right limb bud on opisthosomal segment two (O2) shows four pulmonary furrows (black arrows) and a lateral opening of the pulmonary sac (PuS). At the latero-posterior insertion of the limb bud at opisthosomal segment three (O3), the opening of the tubular trachea (TrO) is visible. e: Posterior opisthosomal region. The anlagen of the left and right tergite plates (Ter) meet dorso-medially (compare with a later stage, Figure 14c). en, endite; L1-L4, walking legs one to four; P, pedipalp; VS, ventral sulcus.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3141654&req=5

Figure 13: Stage 17, Dorsal closure. All scale bars 100 μm. Sytox staining, a-a''', c; SEMs, b, d, e. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared to previous stages (compare with Figure 12a). a': Frontal view. The white arrows indicate the direction of the epidermal and cuticular overgrowth of the brain region. a'': Posterior view. a''': Dorsal view. The white arrows indicate the dorsad growth of tissue that eventually forms the heart (H). b: Dorso-lateral view showing the crumbled appearance of the dorsal tissue directly posterior to the head lobes after dorsal closure. The prosomal tergites continue to extend dorsally (white arrows) (compare with Figure 12a). c: Detail of anterior prosoma. As a result of the forward positioning of the cheliceres and/or posterior positioning of the stomodeum, the labrum (Lb) is now between the bases of the cheliceres (Ch). Cuticular formations (white arrows) are visible in the sternal regions (white asterisks) of the prosomal segments. d: The right limb bud on opisthosomal segment two (O2) shows four pulmonary furrows (black arrows) and a lateral opening of the pulmonary sac (PuS). At the latero-posterior insertion of the limb bud at opisthosomal segment three (O3), the opening of the tubular trachea (TrO) is visible. e: Posterior opisthosomal region. The anlagen of the left and right tergite plates (Ter) meet dorso-medially (compare with a later stage, Figure 14c). en, endite; L1-L4, walking legs one to four; P, pedipalp; VS, ventral sulcus.
Mentions: Dorsal closure completes inversion. The tergites of both body halves meet along the dorsal midline, covering all of the dorsal yolk with embryonic tissue. This gradual event starts posteriorly with the tergites of the caudal region and progresses anteriorly. The laterally expanding tissue of the prosomal tergites meets the tissue posterior to the precheliceral lobes (white arrows; Figure 13b). During the process, the dorsal prosomal surface has a crumpled appearance (Figure 13b). Underneath the area where the tergite plates touch each other, tissue that eventually forms the heart becomes evident (Figure 13a'''). Cuticle covers the sternites in the prosoma (white arrows; Figures 13c) and the brain region is also overgrown by epidermal and cuticular formations (white arrow; Figure 13a'). The embryonic tissue anterior to the pedipalp has bent posteriorly, marking the start of the process in which the supraoesophageal area folds onto the suboesophageal area. As a result of the positioning of the cheliceres and stomodeum, the labrum is positioned between the bases of the cheliceres (Figures 13a'. c). The pedipalps and walking legs have further extended and meet each other medially in a zipper-like manner. The posterior sides of the limb buds on opisthosomal segment two have become concave (Figure 13d). Evident on each bud are four pulmonary furrows (Figure 13d; black arrows) and the opening of the pulmonary sack (Figure 13d; white arrow). The segments posterior to opisthosomal segment eight have become compressed, giving them a swollen appearance (Figure 13e).

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