Segmentation in the Helobdella Body Plan
The leech body plan (Figure 7.1) contains 32 segments, distributed along three tagmata: the head of the animal, including the anterior sucker, which includes four rostral segments, designated R1-R4, respectively, plus non-segmental, prosto- mial structures; the midbody region contains 21 segments, designated M1-M21; and finally the caudal region, associated with the rear sucker contains seven segments, designated C1-C7. The leech body is paradigmatically segmented, featuring spatially coherent metameric structures in derivatives of all three germ layers: ectoderm, mesoderm, and endoderm (Sawyer 1986). Metameric mesodermal derivatives include muscles, nephridia, and even a subset of mesodermally derived neurons. Metameric ectodermal derivatives include the circumferential body wall divisions (annuli) for which the phylum is named, peripheral sensory structures called sensillae, some types of pigment cells, and, most prominently, the ganglia of the ventral nerve cord. Anatomical studies from the 19th century and a large body of neurobiological studies beginning in the 1960s reveals that neurons in the segmental ganglia are uniquely identifiable (in terms of their physiology and morphology) and largely conserved from segment to segment, even across species (Retzius 1891; Muller et al. 1981). Finally, metameric organization of endoderm- derived structures is evidenced by the iterated lobes of the crop (aka cecae in anterior midgut) and of the intestine (posterior midgut). Structures that are not segmented in Helobdella or most leeches include the dorsal anterior ganglion of the nerve cord, the foregut (proboscis and esophagus), salivary glands, ovary, and hindgut (rectum and anus).
Boundary-Driven versus Lineage-Driven Segmentation
Most organisms used to study segmentation are drawn from either arthropods (superphylum Ecdysozoa) or vertebrates (superphylum Deuterostomia). In these
FIGURE 7.1 Segmentation of mesoderm, ectoderm, and endoderm in the Helobdella body plan. This schematic shows a ventral view with anterior up. The rostral and caudal tagmata contain four and seven fused segments (dark blue), respectively, with the latter forming the rear sucker. The midbody tagma consists of 21 separate segments. Segmental muscles are illustrated in Figure 7.4 and are not shown here. Ectodermal segmentation is indicated by: 3 epidermal annuli in each segment (small black bulges, flanked by deeper constrictions of the body wall to mark segment boundaries); bilaterally symmetric ganglia of the ventral nerve cord, linked by connective nerves (small red ovals and red lines, respectively; due to segment fusion, the rostral and caudal tagmata possess larger ganglia (large red ovals) than midbody segments; the nerve cord in midbody segment 21 (dashed oval and line) is obscured by the posterior sucker; segmental components of the peripheral nervous system are not shown. Mesodermal segmentation is indicated by the male genital organs and multiple paired testisacs (orange), which develop in midbody segments 5 and 8-13, respectively; the female reproductive system (purple), originating in midbody segment 6, with ovaries extending posteriorly; the excretory system of paired metanephridia (green) in midbody segments 2-5 and 8-18 (these two sets have reversed orientation relative to one another, filtering coelomic fluid anteriorly and posteriorly, respectively). Endodermal segmentation is indicated by ceca of the midgut, which form distinct segmental evaginations in the crop (taupe) and the intestine (light blue). Non-segmented gut structures include the proboscis and esophagus (yellow) and the rectum (pink).
models, segmentation entails the formation of boundaries that divide fields of (usually) mesodermal or ectodermal cells into metameres. As detailed in Chapter 2, these metameres may arise sequentially (as is the case with vertebrates and short germ insects) or simultaneously (as in long germ insects) along the anterior-posterior (А-P) axis, and may correspond to segmental, parasegmental, or double- segmental primordia. The actual patterns of cell division leading to the formation of morphological pattern elements within the units are often variable (the variable and irregularly shaped clones of cells within Drosophila compartments, for example), and cell clones arising within one metamere are restricted from crossing boundaries separating them from adjacent metameres. This is analogous to creating a repeating pattern in a row of bushes by trimming them so that their branches do not intermingle, without regard for the branching patterns of the individual bushes. We refer to these processes as boundary-driven segmentation mechanisms (Figure 7.2A).
Segmentation by boundary-driven mechanisms is so widespread among the commonly studied animal models that one may be forgiven in assuming that this is the
FIGURE 7.2 Boundary-driven and lineage-driven segmentation. In boundary-driven segmentation (left), as exemplified in arthropods and vertebrates, segmental boundaries are imposed on initially unspecified regions of cells (syncytial blastoderm or presomitic mesoderm). Segmentally iterated structures arise within the segmental boundaries despite variable patterns of cell division, in part due to restrictions on the ability of cells to cross the boundaries. In lineage-driven segmentation (right), as exemplified in leeches and other clitellate annelids, stereotyped patterns of cell division among longitudinally arrayed precursors cells lead to segmentally repeating structures even if their clones interdigitate across morphological segment boundaries.
only way to generate metameres and segments. In fact, however, another process, which we call lineage-driven segmentation, has been described for clitellate annelids and also for malacostracan crustaceans (see Chapter 6). Returning to the analogy of the row of bushes, if the bushes are carefully pruned to achieve the same branching pattern for each bush, then the row of bushes will present a repeating pattern even if the branches of adjacent bushes intermingle (Figure 7.2B). In Helobdella, the metameric structures associated with segmental mesoderm and ectoderm arise in a lineage-driven process as will be described later.
7.4 AN AXIAL POSTERIOR GROWTH ZONE (PGZ)