Research | Spider Development

In all spiders, early development creates a rind of cells that encloses a yolky interior. These outer cells then collect at one side of the spherical egg and the egg contracts at this side (see Movie 3). The result is formation of an embryo that looks like a ball with a flattened side. The flattened side is called the germ disc and it is these cells that will gastrulate to form the primordium of the spider’s body.

Gastrulation is a physical process critical to the normal development of all animal embryos. It converts the simple polarities of the egg into the more complex organization of the later embryo. The main body axes arise during gastrulation as a consequence of the organized movements of cells into the interior. The historical literature on spider development has gastrulation occurring in one continuous phase with two cell types involved. Both cell types internalize at the center of the germ disc via an opening called the blastopore. The first cells to internalize create a small two-layered region called the ‘primitive plate.’ A group of deep cells called the ‘cumulus’ then detaches from the primitive plate and migrates to the edge of the germ disc; the direction of migration will determine the dorsal-ventral axis. During cumulus migration, more superficial cells internalize at the blastopore and these cells migrate toward the periphery to enlarge the primitive plate so that it occupies the entire germ disc. The deep layer of the primitive plate contains the mesoderm and endoderm cells that will make the muscles and gut, respectively. This is the canonical model of spider gastrulation featured in textbooks and reviews, and was derived primarily by reconstructions of fixed specimens. Movie 1 is an animation of this process. Movie 2 is a timelapse of development of Cheiracanthium mildei, a spider that fits the model.

Figure 1

Fig. 1. Canonical spider gastrulation. Blue, blastoderm; orange, primitive plate; yellow, mesoderm and endoderm; red, cumulus. View animation.

The canonical model is being challenged by my lab’s work on Zygiella x-notata (Fig 2 and Movie 4) and the Oda lab’s work on Parasteatoda tepidariorum. My lab combined live imaging techniques with improved fixation methods to show that gastrulation in Zygiella comprises three distinct phases, each of which internalizes a separate population of cells. Surprisingly, the cumulus internalizes first, before the primitive plate. Movie 5 shows the cumulus cells (colored red) internalizing at the central blastopore. The other colored cells represent some of the prospective primitive plate, and they will internalize at the same position some hours later. A third round of internalization will feed cells into the primordium of the posterior body. Zygiella x-notata lives on the Blue Bridge and many other spots on campus.

After gastrulation is complete, another remarkable morphogenetic movement occurs. Inversion involves the splitting of the germ band into left and right halves. The halves move away from each other until they reach the equator (Fig 2, K–M and Movie 3; Fig 3A). Note that the legs elongate during inversion—this can obscure the extent of inversion. Cells then migrate out of the two halves toward the dorsal midline (Fig 3B) while a separate cell sheet envelops the yolk ventrally. ‘Inversion’ is an apt descriptor because cells from the outside edges of the original germ band (red in Fig 3B) meet and fuse at the dorsal midline. The spider dorsal midline, what we normally consider the central axis of an organism, originates at the very outside edges of the embryo.

Figure 2

A–D, Formation of germ disc and cumulus (white arrowhead).
E–H, Migration of cumulus and formation of caudal bud (red arrowhead).
I–L, Migration of caudal bud and consolidation of germ band. Inversion begins: germ band splits into left and right halves. Appendage buds visible.
M–O, Inversion completed. Posterior body enclosed via ventral closure.

Figure 3

A, At the start of inversion, the germ band splits into left and right halves. The ventral sulcus (VS) enlarges as the bands migrate away from each other.

B, At the end of inversion, cells from the outside edges (red) end up at the dorsal midline.

Figure adapted from Foelix, Biology of Spiders.

Very early development of Steatoda grossa embryos appears similar to that of Zygiella. Fig. 4 shows a Steatoda embryo before cellularization. At first, only globules of yolk are visible, but later nuclei can be seen as white areas. The movie shows this period and ends as cells begin to migrate to one side of the egg to form the germ disk.

Subsequent development is somewhat different than that of Zygiella. A single large cellular mass feeds cells into the interior. The cellular mass forms relatively early in development but involves more cells than the Zygiella cumulus. Most cells seem to internalize at one side of the mass. The progress of the leading edge of these cells is outlined by the red line in the stills (Fig. 5). Spiders were obtained from SpiderPharm in Arizona

Figure 4

View movie. A, Only yolk globules are visible early. B, some nuclei (red arrowheads) become visible. Video stills and movie courtesy of Christine Bates ’10.

Figure 5

View movie. The cellular mass of Steatoda feeds cells into the interior of the embryo. The progress of the leading edge of these cells is outlined by the red line. Video stills and movie courtesy of Emily Vance '05.