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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 15, Inversion II. All scale bars 100 μm. Sytox staining, a-a''; SEMs, b, c. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared with previous stages (see Figure 10a). a': Frontal view. The white dotted line indicates the mouth opening between the two lateral subdivisions of the developing brain (compare with Figure 10a'). The two labral lobes have completely fused and the labrum (Lb) is now an unpaired structure. a'': Posterior view. The white dotted line shows the progress of inversion (middle diagram in d). b: Opisthosomal region. Separated opisthosomal segments four to nine (O4-9) are visible. The tenth (O10) and the future eleventh segments (black dotted line) are located together with the growth zone (GZ) in a tail-like portion of the germ band that protrudes from the mass of yolk. Small bulges of tergite anlagen (Ter) are evident on the dorsal surface (compare with the more differentiated tergite anlagen in Figure 14c). c: Detail of the right third and fourth walking legs (L3, L4) and the limb buds of opisthosomal segments two and three (O2, O3). At the posterior base of the limb bud of O2 the opening of the pulmonary sac (white arrow) is seen, and adjacent to it medially are two slit-like openings (black arrows) to the book lungs. The podomeres of the fourth walking leg (L4) are numbered (1-5) from base to tip. d: Schematic illustration of the steps of inversion corresponding to stages 14 (compare with Figure 10 a''), 15 (compare with Figure 11 a''), and 16 (compare with Figure 12 a''). Posterior view, dorsal is at the top of the diagrams. The germ band (brown areas) has divided, and the ventral sulcus (VS) is increasing in width. The bilateral regions of the germ band are migrating dorsally (black arrows), enclosing the yolk area (Y) and eventually meeting in the dorsal midline (stage 17, dorsal closure). By stage 15, the dorsal edges of both halves of the germ band lie in a line when viewed from posterior. AF, anterior furrow; Ch, chelicere; P, pedipalp; X, damaged area, cuticle torn.
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Figure 11: Stage 15, Inversion II. All scale bars 100 μm. Sytox staining, a-a''; SEMs, b, c. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared with previous stages (see Figure 10a). a': Frontal view. The white dotted line indicates the mouth opening between the two lateral subdivisions of the developing brain (compare with Figure 10a'). The two labral lobes have completely fused and the labrum (Lb) is now an unpaired structure. a'': Posterior view. The white dotted line shows the progress of inversion (middle diagram in d). b: Opisthosomal region. Separated opisthosomal segments four to nine (O4-9) are visible. The tenth (O10) and the future eleventh segments (black dotted line) are located together with the growth zone (GZ) in a tail-like portion of the germ band that protrudes from the mass of yolk. Small bulges of tergite anlagen (Ter) are evident on the dorsal surface (compare with the more differentiated tergite anlagen in Figure 14c). c: Detail of the right third and fourth walking legs (L3, L4) and the limb buds of opisthosomal segments two and three (O2, O3). At the posterior base of the limb bud of O2 the opening of the pulmonary sac (white arrow) is seen, and adjacent to it medially are two slit-like openings (black arrows) to the book lungs. The podomeres of the fourth walking leg (L4) are numbered (1-5) from base to tip. d: Schematic illustration of the steps of inversion corresponding to stages 14 (compare with Figure 10 a''), 15 (compare with Figure 11 a''), and 16 (compare with Figure 12 a''). Posterior view, dorsal is at the top of the diagrams. The germ band (brown areas) has divided, and the ventral sulcus (VS) is increasing in width. The bilateral regions of the germ band are migrating dorsally (black arrows), enclosing the yolk area (Y) and eventually meeting in the dorsal midline (stage 17, dorsal closure). By stage 15, the dorsal edges of both halves of the germ band lie in a line when viewed from posterior. AF, anterior furrow; Ch, chelicere; P, pedipalp; X, damaged area, cuticle torn.

Mentions: The gradual widening of the ventral sulcus, which from stage 11 to 13 is a relatively slow process, significantly accelerates during stage 14 (Figures 10a'', e). This marks the start of inversion, a complex sequence of tissue movement and growth that results in a rearrangement of the body and incorporation of the yolk mass into the embryo. Apart from the precheliceral region and the posterior-most opisthosomal segments, the two halves of the germ band move separately over the yolk mass until they connect again on the dorsal side (Figure 11d gives a schematic overview). As a result of this movement, the distance between the precheliceral region and the posterior opisthosomal region increases. Simultaneously, the germ band continues to extend with the addition of the final opisthosomal segments. The precheliceral region, which until inversion was an extension of the rest of the germ band, gradually folds posteriorly. In order to precisely map the various developmental events that occur during inversion, we distinguish four separate stages.


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

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

Stage 15, Inversion II. All scale bars 100 μm. Sytox staining, a-a''; SEMs, b, c. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared with previous stages (see Figure 10a). a': Frontal view. The white dotted line indicates the mouth opening between the two lateral subdivisions of the developing brain (compare with Figure 10a'). The two labral lobes have completely fused and the labrum (Lb) is now an unpaired structure. a'': Posterior view. The white dotted line shows the progress of inversion (middle diagram in d). b: Opisthosomal region. Separated opisthosomal segments four to nine (O4-9) are visible. The tenth (O10) and the future eleventh segments (black dotted line) are located together with the growth zone (GZ) in a tail-like portion of the germ band that protrudes from the mass of yolk. Small bulges of tergite anlagen (Ter) are evident on the dorsal surface (compare with the more differentiated tergite anlagen in Figure 14c). c: Detail of the right third and fourth walking legs (L3, L4) and the limb buds of opisthosomal segments two and three (O2, O3). At the posterior base of the limb bud of O2 the opening of the pulmonary sac (white arrow) is seen, and adjacent to it medially are two slit-like openings (black arrows) to the book lungs. The podomeres of the fourth walking leg (L4) are numbered (1-5) from base to tip. d: Schematic illustration of the steps of inversion corresponding to stages 14 (compare with Figure 10 a''), 15 (compare with Figure 11 a''), and 16 (compare with Figure 12 a''). Posterior view, dorsal is at the top of the diagrams. The germ band (brown areas) has divided, and the ventral sulcus (VS) is increasing in width. The bilateral regions of the germ band are migrating dorsally (black arrows), enclosing the yolk area (Y) and eventually meeting in the dorsal midline (stage 17, dorsal closure). By stage 15, the dorsal edges of both halves of the germ band lie in a line when viewed from posterior. AF, anterior furrow; Ch, chelicere; P, pedipalp; X, damaged area, cuticle torn.
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Related In: Results  -  Collection

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Figure 11: Stage 15, Inversion II. All scale bars 100 μm. Sytox staining, a-a''; SEMs, b, c. a: Lateral view. The white line indicates the increased distance from the precheliceral lobes (PcL) to the opisthosomal tail compared with previous stages (see Figure 10a). a': Frontal view. The white dotted line indicates the mouth opening between the two lateral subdivisions of the developing brain (compare with Figure 10a'). The two labral lobes have completely fused and the labrum (Lb) is now an unpaired structure. a'': Posterior view. The white dotted line shows the progress of inversion (middle diagram in d). b: Opisthosomal region. Separated opisthosomal segments four to nine (O4-9) are visible. The tenth (O10) and the future eleventh segments (black dotted line) are located together with the growth zone (GZ) in a tail-like portion of the germ band that protrudes from the mass of yolk. Small bulges of tergite anlagen (Ter) are evident on the dorsal surface (compare with the more differentiated tergite anlagen in Figure 14c). c: Detail of the right third and fourth walking legs (L3, L4) and the limb buds of opisthosomal segments two and three (O2, O3). At the posterior base of the limb bud of O2 the opening of the pulmonary sac (white arrow) is seen, and adjacent to it medially are two slit-like openings (black arrows) to the book lungs. The podomeres of the fourth walking leg (L4) are numbered (1-5) from base to tip. d: Schematic illustration of the steps of inversion corresponding to stages 14 (compare with Figure 10 a''), 15 (compare with Figure 11 a''), and 16 (compare with Figure 12 a''). Posterior view, dorsal is at the top of the diagrams. The germ band (brown areas) has divided, and the ventral sulcus (VS) is increasing in width. The bilateral regions of the germ band are migrating dorsally (black arrows), enclosing the yolk area (Y) and eventually meeting in the dorsal midline (stage 17, dorsal closure). By stage 15, the dorsal edges of both halves of the germ band lie in a line when viewed from posterior. AF, anterior furrow; Ch, chelicere; P, pedipalp; X, damaged area, cuticle torn.
Mentions: The gradual widening of the ventral sulcus, which from stage 11 to 13 is a relatively slow process, significantly accelerates during stage 14 (Figures 10a'', e). This marks the start of inversion, a complex sequence of tissue movement and growth that results in a rearrangement of the body and incorporation of the yolk mass into the embryo. Apart from the precheliceral region and the posterior-most opisthosomal segments, the two halves of the germ band move separately over the yolk mass until they connect again on the dorsal side (Figure 11d gives a schematic overview). As a result of this movement, the distance between the precheliceral region and the posterior opisthosomal region increases. Simultaneously, the germ band continues to extend with the addition of the final opisthosomal segments. The precheliceral region, which until inversion was an extension of the rest of the germ band, gradually folds posteriorly. In order to precisely map the various developmental events that occur during inversion, we distinguish four separate stages.

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