Cell Lineage and Cell Fate
It has been suggested that stereotyped cell division patterns during embryonic development indicate cell autonomous differentiation (e.g., Stent 1985; Weisblat and Shankland 1985). According to this view, cells gain the instructions for their further
FIGURE 6.12 Cell ablation experiments in the decapod Cheraxdestructor. The dark brown cells express engrailed. The loss of cellular material in early germ bands by injection of thin glass electrodes led to a number of different malformations. (A and B) Ventral and dorsal aspects of an embryonic pleon showing spiral segmentation (helicomery). The engrailed stripe of the third pleonic segment anlage (pl3) is medially interrupted and somewhat shifted. At the dorsal level the stripe is intact. On the animal’s right side, it is connected to the fourth pleonic stripe (pl4), which continues at the dorsal side and is ventrally confluent with the fifth pleonic segment anlage (pl5). Thus, a spiral with two loops is formed. (C) A more dramatic loss of cellular material resulting in a very thin pleon, which nevertheless shows a more or less regular engrailed expression. The posterior thoracic segments are completely distorted and fused with a greatly irregular engrailed pattern. (D) A normally developed pleon in a corresponding stage for comparison.
fate based on the lineage that led to their existence. Thus, the teloblasts are thought to imprint a specific fate on their descendant cells. This view has been put forward based on experimental studies on clitellate worms (Shankland 1991; Shankland and Savage 1997). Like malacostracans but convergently (see Scholtz 2002), Clitellata differentiate ecto- and mesoteloblasts that give rise to columns of cells with a specific cell fate during the formation of segmental structures (Storey 1989; Shankland and Savage 1997). However, the comparative data of malacostracan germ bands are ambivalent. The fact that the cells of non-ectoteloblastic origin anterior to the first ectoteloblast show a corresponding division pattern and adopt the same fate as the latter suggests that it is more the region rather than the origin that influences cell differentiation (Scholtz and Dohle 1996). By contrast, cell ablation and perturbation experiments in Cherax destructor embryos shortly after the formation of the telo- blast rings using fine glass electrodes and the application of the engrailed antibody suggest that at least in teloblast descendants, the fate seems determined by their origin. These experiments resulted in extremely malformed germ bands with different patterns. Two examples are shown here (Figure 6.12). One embryo possesses a very thin posterior region. At the transition between the unaffected and the distorted region engrailed expression is clustered and does not show a regular segmental pattern. By contrast, the expression pattern in the narrow posterior region is quite regular, comparable to the situation in normal embryos of that stage (Figure 6.12C, D). The other embryo shows a case of spiral segmentation or helicomery (see Morgan 1895; Lesniewska et al. 2009; Scholtz 2017) (Figure 6.12A, B). This phenomenon occurs if in the area of a segment anlage one half is shifted out of phase and thus connected with an adjacent segmental half, creating one or more spiral loops around the body (see Chapter 1). These results indicate that engrailed expression is based on cell lineage. The cells maintain engrailed expression despite being out of register compared to the wild-type condition and lying in close contact to other engrailed positive cells. The same explanation holds true for the spiral segments. The displacement of cells does not alter their fate as engrailed positive cells. The expression pattern in the narrow posterior end can be explained by a low number of remaining ectoteloblasts, which nevertheless produce a normal pattern of descendants.
Yet, this conclusion concerns only the normal differentiation processes during the embryonic development of recent species. If the course of evolution is considered, the causal connection of ontogenetic stages can be dramatically altered (Scholtz and Dohle 1996; Scholtz 2008). One example is the loss of ectoteloblasts in amphipods, in which ectoteloblasts are not a necessary prerequisite for the regular row arrangement and the stereotyped cleavage pattern in the malacostracan germ band. In other words, the tight relation between teloblasts and the fate of their descendants has been evolutionarily decoupled.