Kinship Groups Are Well Conserved within Each Lineage, But Heterogeneous in Terms of Cell-Type Composition and Spatial Distribution

Among the four ectodermal lineages (N, О, P, and Q), the N kinship group (defined in Section 7.5) is primarily composed of neurons in the ventral ganglia, while the Q kinship group constitutes primarily dorsal epidermis, while the О and P kinship groups contribute primarily ventrolateral and dorsolateral ectoderm (Figure 7.4), respectively. There is extensive mediolateral intercalation among the kinship groups, however. Even the dorsalmost (Q) kinship group contributes a small set of neurons to the ventral ganglion (Weisblat et al. 1984). These cells arise by a small set of precursors that separate from the main Q lineage and migrate medially within the germinal plate (Torrence and Stuart 1986). For the giant glossiphoniid leech species, Haementeria ghilianii, it has been possible to combine lineage tracing with neurophysiological characterization of individual neurons in the segmental ganglia of late- stage embryos. This approach has confirmed that individually identified neurons arise from specific kinship groups (Kramer and Weisblat 1985), and these lineage relationships appear to be conserved at least across glossiphoniid species. Moreover, the distinct patterns of teloblast-derived ectodermal kinship groups can also be recognized in oligochaetes (Goto et al. 1999a, 1999b; Arai et al. 2001; Storey 1989a, 1989b), indicating that many of the cellular details of segmentation via a teloblastic growth are conserved from an ancestral clitellate annelid.

Kinship Groups Are Not Clones

What is the spatial relationship between a teloblast’s kinship group (i.e., all the descendants of that teloblast that occur within one morphologically defined segment) and the blast cell clones in that teloblast lineage (i.e., all the descendants of individual blast cells)? To characterize the segmental contributions of individual blast cells, the blast cells themselves can be injected with lineage tracers in Helobdella or related species (M. Leviten, unpublished observations; Gleizer and Stent 1993; Shankland 1987a; Shain et al. 1998; Kuo and Shankland 2004a), albeit only with considerable difficulty. An alternative method for following the fates of individual blast cells is to inject the same teloblast during successive cell cycles with two different tracers, thereby labeling one individual blast cell uniquely (Zackson 1982; Gline et al. 2011; Kuo and Shankland 2004a). A third way to examine the distribution of individual blast cell clones is to inject a teloblast with tracer after it has already produced some blast cells, and then examine the distribution of progeny at the boundary between the last unlabeled and first labeled blast cells in the lineage (Weisblat and Shankland 1985).

Stereotyped spatial distribution of blast cell clones in parental and grandparental stem cell lineages

FIGURE 7.4 Stereotyped spatial distribution of blast cell clones in parental and grandparental stem cell lineages. Schematic representation of the Helobdella PGZ (lower portion of drawing) and germinal plate (upper portion), depicting the anteroposterior progression of segmentation in terms of individual blast cell clones. For simplicity, only the mesodermal (M) lineage is shown in the left side of the figure and only the four ectodermal (N, О, P, Q) lineages are shown in the right side of the figure; the ventral midline is indicated by the dotted line at the center of the drawing, while the edges correspond to the dorsal midline. In the mesodermal (M teloblast) lineage (pink), individual blast cells initiate their stereotyped pattern of divisions prior to entering the germinal band. Each cell makes one segment’s worth of definitive progeny, including body wall muscles, nephridia, and a few ganglionic neurons, but the final clone of cells arising from a single m blast cell is distributed over three segments. The О and P lineages arise from initially equipotent О/P teloblasts and blast cells, which assume distinct О (orange) and P (yellow) fates within the germinal bands (see Figure 7.3). Individual о and p blast cell clones make one segment’s worth of definitive progeny for ventrolateral and dorsolateral ectoderm, respectively, including specific sets of ganglionic neurons, epidermis, and peripheral neurons, but the final clones of cells are distributed over two morphological segments. The N (blue) and Q (green) lineages also contribute specific sets of ganglionic neurons, epidermis, and peripheral neurons to ventral and dorsal ectoderm, respectively, but in each of these lineages, two blast cell clones are required to make a single segment’s worth of definitive progeny.

These overlapping and complementary approaches have revealed that in contrast with arthropod and vertebrate models, leech segmentation is a lineage-driven process and not a boundary-driven one. Specifically, for the M, O, and P lineages, serially homologous blast cell clones within the same lineage interdigitate longitudinally. Thus, the differentiated cell types (definitive progeny) that make up one blast cell’s mature clone are distributed across more than one morphologically defined segment, and the set of cells in each segment that comprise the M, O, or P kinship group arise from more than one blast cell clone (Figures 7.2 and 7.4).

For example, the O-lineage neurons on the left side of each segmental ganglion arise from two different о bandlet blast cells (Figure 7.4) (Weisblat and Shankland 1985). For the mesodermal (M) lineage, the situation is even more extreme—the progeny of individual m blast cell clones are distributed longitudinally over three consecutive segments (Figure 7.4). Overall, it is difficult if not impossible to reconcile these results with the compartment model of segmentation that has been applied to arthropod taxa, but they are fully consistent with the notion of lineage-driven segmentation.

Obviously this conclusion breaks down at the anterior and posterior ends of the animal, where there is no “next” segment to which cells can migrate and no “next blast cell” from which they migrate. The full details of how blast cell lineages are altered in these regions remains to be determined, but careful application of lineage tracing techniques has provided partial answers. For example, in the early mesodermal (M) lineage, the first six m blast cells (designated eml through em6, respectively) contribute progeny to a variety of non-segmental tissues (Gline et al. 2011). Of these six cells, eml through em4 make no contributions at all to segmental mesoderm; em5 and em6, however, each generate a clone that is a hybrid of segmental and non-segmental progeny. Specifically, they contribute progeny to the first two mesodermal segments, segments R1 and R2, that in midbody segments would be produced by anterior m blast cells.

 
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