Like hexapods, myriapods, and chelicerates, non-malacostracan crustaceans do not show' specific cell types in their growth zone. Furthermore, the cells in the germ band do not display a recognizable stereotyped pattern of cell division and arrangement. This is different in malacostracans. They show individually recognizable cells and reproducible cell division patterns during the formation and differentiation of the germ band up to early segmentation. Parts of this idiosyncratic developmental process w'ere detected in the 19th century. Reichenbach (1886) was the first to describe the special stem cells of the growth zone of malacostracans, the ectodermal teloblasts, and Patten (1890) reported similar cells in the mesoderm, the mesoteloblasts (Figure 6.2A. B). Bergh (1893, 1894) and McMurrich (1895) were the first to resolve aspects of the regular stereotyped cleavage pattern in the malacostracan germ band. Since then, the stereotyped formation and differentiation of the malacostracan germ band (see Figures 6.2-6.7) has been intensely studied, leading to the most detailed knowledge of the early segmentation process in crustaceans (Dohle et al. 2004).

The growth zone of most Malacostraca is characterized by transversely arranged relatively large stem cells, the teloblasts (Figures 6.2-6.7). As mentioned earlier, teloblasts occur in the ectoderm (ectoteloblasts) and mesoderm (mesoteloblasts). They divide asymmetrically producing smaller cells in an anterior direction (Figures 6.2 and 6.5—6.7). This generates the cellular material for the subsequent segmentation of the germ band. A ring of 19 ectoteloblasts (one unpaired ventral median ectoteloblast and nine paired ectoteloblasts on either side of the midline) and an inner ring of 8 mesoteloblasts (four on either side, a median mesoteloblast is absent) that surround the caudal papilla anterior to the telson anlage are found in Leptrostraca, Stomatopoda, most Decapoda, Euphausiacea, Anaspidacea, and Thermosbaenacea (Scholtz 2000) (Figures 6.2C and 6.3A). This distribution allows for the conclusions that this pattern is the original condition for Malacostraca (Scholtz 2000). How'ever, w'ithin malacostracans some evolutionary changes have taken place. In the lineage to freshwater crayfishes, the number of ectoteloblasts increased to about 40 and the ring arrangement persisted (Scholtz 1993; Scholtz et al. 2009) (Figure 6.2D). In contrast to this, the teloblast rings have been evolutionarily transformed to transverse rows with a variable number (15-23) of ectoteloblasts in Peracarida (Figure 6.2E). The Amphipoda are a notable exception, because they lost ectoteloblasts entirely (Bergh 1894; Scholtz and Wolff 2002) (Figure 6.2F). In contrast to the situation in ectoteloblasts, the mesoteloblasts remain conservative, and no exception of the number 8 has been found (Figures

6.2 and 6.4). Even amphipods that evolutionarily lost ectoteloblasts are equipped with 8 mesoteloblasts (Figure 6.4). The only evolutionary change in mesoteloblasts occurs in peracarids, w'hich show' a transverse row' of mesoteloblasts instead of the plesiomor- phic ring arrangement (Scholtz 2000) (see Figures 6.2В, 6.5C, and 6.7).

Differentiation of ectoteloblasts

FIGURE 6.3 Differentiation of ectoteloblasts. (A) The complex cell division pattern during the differentiation of ectoteloblasts in one body half in some decapod crustaceans (modified after Ooishi 1959, with permission from Wiley & Sons). The Roman numerals label ectotelo- blast precursors; the ectoteloblasts are designated with an uppercase E and their descendants with lowercase e. (B) The in situ formation of ectoteloblasts in the early germ disc of the cumacean Diastylis rathkei (modified after Dohle 1970, with permission from Springer). The ectoteloblasts form two half rings that migrate around the gastrulation center (immigrated cell are shown as dark and dotted nuclei) and meet anteriorly in the middle. One of the cells between the two first ectoteloblasts (ET,) will be transformed into the median, unpaired ectoteloblast. (C) The formation of ectoteloblasts (ET) in the early germ disc of the decapod Cherax destructor. As in the cumacean (B) and in contrast to other decapods, the ectoteloblasts of crayfish differentiate in situ. This happens during the formation of the caudal papilla (cp) and the proctodaeum (pr) at a stage where the naupliar appendages begin to differentiate, as is exemplified by the mandibular buds (md) (compare with Figure 6.IB). One of the midline cells (ml) will become the median unpaired ectoteloblast (see Figure 6.2D, ET0).

Differentiation of rnesoteloblasts

FIGURE 6.4 Differentiation of rnesoteloblasts. (A) The cell division pattern of the differentiation of rnesoteloblasts in one body half of some decapods (modified after Ooishi 1959, with permission from Wiley & Sons). M labels rnesoteloblasts (Arabic numerals) and mesotelo- blast precursors (Roman numerals). The mesoteloblast descendants are labeled with a lowercase m. Corresponding patterns in (B) the cumacean Diastylis rathkei (modified after Dohle et al. 2004) and (C) the amphipod Gammarus pulex (modified after Scholtz 1990). In both cases rnesoteloblasts (Arabic numerals) and their precursors (Roman numerals) are labeled MT, the descendants are designated with lowercase m. (D) The germ disc of the amphipod Gammarus pulex at the transition to a germ band showing the subectodermal position of the mesoteloblasts/precursors) (MT) (modified after Scholtz 1990). Posterior to the dorsal organ (do) are the head lobes (hi; compare with Figures 6.1 and 6.2). The first transverse ectoderm rows are forming (lines).

Ectoteloblasts are generated in several different ways. Ooishi (1959, 1960) described a complex stereotyped cell division pattern for a decapod shrimp, a hermit, and a brachyuran crab (Figure 6.3). In these species, the ectoteloblasts are differentiated in a stepwise manner and the most ventral ectoteloblasts begin their characteristic asymmetric divisions before the more dorsal ectoteloblasts have been differentiated. The ectoteloblasts in a freshwater crayfish and a cumacean have been reported to form in situ without any special lineage but nevertheless in a ventral-dor- sal sequence (Dohle 1970; Scholtz 1992). By contrast, the differentiation of meso- teloblasts follows a cell lineage in decapods, cumaceans, and amphipods (Ooishi 1959, 1960; Dohle 1970; Scholtz 1990; Price and Patel 2008; Hunnekuhl and Wolff

2012) (Figure 6.4).

With their asymmetric divisions, the teloblasts generate regular transverse rows or rings of cells that form a regular gridlike pattern (Hejnol et al. 2006). The divisions of the teloblasts follow more or less a mediolateral wave of mitoses on either side of the midline (Figure 6.5B). The unpaired median ectoteloblast generates a midline column of unpaired cells that matches the symmetry axis of the body in the post-naupliar region (Figure 6.5B). Each ectodermal transverse row or ring of ectoteloblast derivatives forms a genealogical unit (Figures 6.5 and 6.6). In the ectoderm, the cells of each of these rows divide twice following a mediolateral wave of mitoses with an anteroposterior spindle orientation (Dohle et al. 2004; Scholtz and Wolff

2013) (Figures 6.5 and 6.6). Each row generates four descendant rows, which are still arranged in a regular grid (Figures 6.5 and 6.6). This process elongates the germ band further. Hence, germ band elongation is a two-step process: first the generation of ectoteloblast rows (founders of the genealogical units), second the two waves of divisions in longitudinal direction of each of these rows (Scholtz and Wolff 2013) (Figures 6.5B, C and 6.6). After that the differential cleavages begin. These mitoses have varying spindle orientations and are sometimes asymmetric but nonetheless still follow a stereotyped pattern (Figures 6.5 and 6.6). With these differential cleavages, the germ band becomes three-dimensional and the segmental structures such as intersegmental furrows, limb buds, and ganglion primordia are formed (Dohle et al. 2004) (Figures 6.5, 6.6, and 6.11).

When the gridlike arrangement of the ectoderm cells was detected, it was thought that each of the ectoteloblast transverse rows or rings gave rise to a morphological adult segment (Bergh 1893; McMurrich 1895; Manton 1928). However, more detailed analyses have shown that the segmental boundaries run transversely and slightly obliquely through the progeny of each ectoteloblast row (Dohle 1972, 1976; Scholtz 1984: Dohle and Scholtz 1988; Scholtz and Dohle 1996). Hence, every morphological segment in the ectoderm is formed by the progeny of two genealogical units and likewise segmental ganglia and legs are composite structures (Dohle et al 2004) (Figures 6.5, 6.6, and 6.11). Interestingly, amphipods show the same regular pattern of the ectoderm cells in the germ band despite the absence of ectoteloblasts (Scholtz 1990; Dohle et al. 2004). In this case, the rows form by an arrangement of previously scattered ectodermal cells in an anteroposterior sequence (Figures 6.2F, 6.5C, D, and 6.6).

It appears that the midline cells play an organizing role during the process of row generation and segment differentiation. This is indicated by the early and accelerated formation of the midline propagating in the anteroposterior direction and the subsequent generation of ectoderm rows from the midline toward lateral (Scholtz 1990). Experiments in which midline cells of the amphipod Parhyale hawaiensis have been ablated with laser beams and the expression of the single-minded (sim) gene has been suppressed strongly corroborated this view. Both approaches led to

The germ bands of a cladoceran and three malacostracans

FIGURE 6.5 The germ bands of a cladoceran and three malacostracans. The first thoracic segment (thl) is labeled for comparison. Parts A-C are camera lucida drawings (A is modified after Gerberding 1997; В and C are modified after Scholtz 1984, 1990). Part D is a fluorescent staining of cell nuclei with Bisbenzimide (Hoechst Blue). (A) The post-naupliar germ band of the cladoceran Leptodora kindtii. There are many small cells with an irregular arrangement, and ectoteloblasts are lacking. (B) Germ band of Neomysis integer. There are relatively few cells, which are regularly arranged in a gridlike pattern of longitudinal columns (including a midline) and transverse rows. The large ectoteloblasts (arrow) give rise to regular rows that follow a determined sequence of division (yellow: undivided rows; blue: rows in the phase of the first wave of division; green: rows in the phase of the second wave of division; orange: beginning differential cleavages and morphological segmentation; red: the offspring of one ectoteloblast along the anteroposterior axis of the germ band), ie, intercalary elongation; sb, segmental border; gb, genealogical boundary (for explanation see text). In malacostracans, the telson is formed posterior to the teloblasts. (C) The advanced germ band of the amphipod Gammaruspulex. In this case, the regular gridlike pattern of ectoderm cells forms without ectoteloblasts. This is an apomorphy of Amphipoda. The midline is omitted; the mesoderm is drawn in bold lines. The eight mesoteloblasts (MT) at the end of the germ band and the transverse rows of mesoteloblast derivatives are visible (numbers in brackets). Some individual cells of the mesoderm are labeled. (D) The post-naupliar germ band of the amphipod Cryptorchestia garbinii showing the regular cell arrangement. The stage is slightly younger than that in (C).

Schematic summary of row formation and segmentation in the post-naupliar germ band of malacostracan crustaceans

FIGURE 6.6 Schematic summary of row formation and segmentation in the post-naupliar germ band of malacostracan crustaceans. Only the animal’s left side is shown and the midline is on the left side. Transverse lines indicate the genealogical borders (gb) between the ectoderm rows. The transverse ectoderm rows are formed either by ectoteloblasts (ET), a condition found in the posterior part of most peracarids and decapods examined (A), or by scattered blastoderm cells (B), a condition found in anterior rows of most peracarids and decapods and in the entire post-naupliar germ band in amphipods. After formation, each row (except the anteriormost rows that show a somewhat different pattern) undergoes two medio- lateral mitotic waves with only longitudinally oriented spindles and equal mitoses, resulting in four transverse descendant rows named a, b, c, d (C, D). Thereafter, the differential cleavages begin. These show a stereotyped pattern of mitoses with regard to size and position of the division products. (E) A simplified schematic pattern of the first differential cleavage up to the fifth cells from the midline. Some characteristics of the individual mitoses differ among the studied species, a phenomenon not shown here (for comparison see Dohle et al. 2004). With the differential cleavages, segmentation begins. The segmental boundary (shaded area) marked by the intersegmental furrow (if) does not match the genealogical border (gb). The intersegmental furrows run transversely and slightly obliquely through the descendants of one ectoderm row in the area of descendant rows a and b (compare with Figure 6.11). Thus, the descendants of each ectoderm row contribute to two segments.

Mesoteloblast and their descendants (modified after Wolff and Scholtz 2002, with permission from Elsevier). The result of the in vivo labeling of two blastomeres of the 16-cell stage (insert

FIGURE 6.7 Mesoteloblast and their descendants (modified after Wolff and Scholtz 2002, with permission from Elsevier). The result of the in vivo labeling of two blastomeres of the 16-cell stage (insert: red cells) of Cryptorchestia garbinii with the fluorescent dye Dil. The eight mesoteloblast (MT), their descendant transverse rows (beginning at the first maxillary segment [mxl]) and the endodermal midgut-gland anlagen (en) are stained. The cells of the more anterior mesoderm rows begin their first wave of division with slightly oblique spindle orientations.

a dorsalization of ventral areas of the germ band (Vargas-Vila et al. 2010). The sim gene is known from Drosophila to play a role in the differentiation of midline and ventral cell fates (see Vargas-Vila et al. 2010). Apparently, a mediolateral gradient of sim is also responsible for the ventrodorsal differentiation of segmental structures in the amphipod Parhyale hawaiensis (Vargas-Vila et al. 2010). In malacostracans with ectoteloblasts, the role of the midline must begin with the differentiation of the median ectoteloblast cell. The latter produces most of the midline cells in an anterior direction (Dohle et al. 2004).

The mesoderm rows show a much larger distance between each other and undergo a different sequence of mitoses. Furthermore, there is no unpaired midline population as in the ectoderm. Nevertheless, the mesoderm cells also reveal a stereotyped arrangement and cell division pattern (Dohle 1972; Scholtz 1990; Price and Patel 2008; Hunnekuhl and Wolff 2012) (Figures 6.2B and 6.7). In contrast to the ectoderm rows, each mesoteloblast row generates the mesodermal equipment of one morphological segment. Hence, in the mesoderm the genealogical units and the segments match. There is only one curious exception, which has been described in two amphipod species. This involves the innermost-paired mesoderm cells of the first thoracic segment. These are generated in the second maxillary segment and migrate posteriorly, joining the mesoteloblasts descendants of the first thoracic segment to form the full complement of four mesoderm cells per side (Scholtz 1990; Price and

Patel 2008). The segmental mesoteloblast descendant cells of each side form the ventral body musculature (innermost mesoteloblast derivatives), the muscles of the limb (the two median mesoteloblast derivatives), and the dorsal heart (the most lateral mesoteloblast derivatives) (Hunnekuhl and Wolff 2012).

The teloblasts do not generate the material for all segments. The cells of the prospective naupliar region are formed before the teloblasts are differentiated. Ectodermal and mesodermal cells seem irregularly distributed and a stereotyped cell lineage cannot be identified (Dohle et al. 2004; Scholtz and Wolff 2013). In addition, the ectodermal cells giving rise to the segments of the first and second maxillae and the anterior part of the first thoracic segment do not descend from the ecto- teloblasts. Nevertheless, they are arranged in transverse rows like the ectoteloblast derivatives and they show a similar further cell division pattern, with the notable exception of the anterior part of the first maxilla, which shows a slightly different cell arrangement and division pattern (Dohle et al. 2004; Wolff and Scholtz 2006). After the formation of 12 rows in the cumacean Diastylis rathkei or 13 ectoderm rows in the decapod Cherax destructor, the ectoteloblasts quit their characteristic asymmetric divisions. Two more rows are formed with somewhat more irregular divisions, which produce the cells for the transition between the last segment and the telson (Dohle 1970; Scholtz 1992).

The post-naupliar mesoderm behaves differently. Descendants of mesoteloblast precursors and differentiated mesoteloblasts form the mesodermal equipment of the post- naupliar segments beginning with the second maxilla (Hunnekuhl and Wolff 2012). Yet, as in the ectoteloblasts, the final divisions of the mesoteloblasts are either inverted with respect to the smaller daughter cells or symmetrical (Dohle 1970; Scholtz 1990). Whether derivatives of mesoteloblast contribute to the telson mesoderm is not clear.

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