Expression of the engrailed gene reveals nine putative segment-anlagen in the embryonic pleon of the freshwater crayfish cherax destructor (Crustacea, Malacostraca, Decapoda).
The Malacostraca constitutes a monophyletic taxon well defined by several apomorphic characters such as a characteristic tagmosis, the position of the gonopores, the subdivision of the stomach into specific functional units, and a ring of 19 embryonic ectoteloblasts (for review and discussion of different views see Dahl, 1992; Wagele, 1992). Within the Malacostraca, the Leptostraca possess a pleon (abdomen) consisting of seven segments and a telson. In contrast to all anterior segments, the seventh pleonic segment is limbless. The other malacostracan groups, unified as the Eumalacostraca (sensu Grobben, 1892), have only six pleomeres, all equipped with limbs. The posteriormost limbs are the uropods which, together with the flattened telson, form the tail fan. The general view is that the pleon of the Leptostraca represents the plesiomorphic condition, and the loss of a pleon segment and the evolution of the tail fan are considered to be derived characters of the Eumalacostraca (e.g., Lauterbach, 1975; Hessler, 1983). However, there has been some controversy over which pleomere has been lost in the course of evolution and to which segment the uropods belong. On the basis of anatomical and paleontological data, Siewing (1956, 1963) argued that the uropods might be the appendages of the seventh pleomere and that the sixth (penultimate) pleomere has been lost in most eumalacostracans. Based on her embryological studies in mysidaceans, Manton (1928a, b), in contrast, suggested that the uropods belong to the sixth pleomere and that the original seventh is fused to the sixth pleomere. Although it was shown in the meantime that paleontological data do not support Siewing's suggestions (Dahl, 1983) - and although Manton's view has been adopted by many carcinologists such as Lauterbach (1975), Hessler (1983), and Dahl (1992) - the problem is still far from being settled (see, for instance, the discussion after the 1983 paper by Hessler) and a different approach seemed to be required to clarify this issue.
Within the arthropods, insects and crustaceans have the segment-polarity gene engrailed already expressed in transverse stripes at the posterior margin of embryonic segments before morphogenesis takes place (e.g., Patel et al., 1989; Manzanares et al., 1993; Scholtz et al., 1993, 1994; Patel, 1994). Therefore, it is a suitable marker for the analysis of the terminal regions of arthropods where segmentation is obscured by morphological rearrangements and the loss of segmental structures in the adult. Several studies have used engrailed to analyze the segmentation of the head in insects and crustaceans (e.g., Fleig, 1994; Schmidt-Ott et al., 1994; Scholtz, 1995), but the caudal segments have been analyzed only in insects (e.g., Kuhn et al., 1992; Schmidt-Ott et al., 1994).
In the present investigation, I used the anti-engrailed antibody mAb 4D9 (Patel et al., 1989) to analyze the segmentation of the embryonic pleon of a eumalacostracan, the Australian freshwater crayfish Cherax destructor. I found that, posterior to the six pleomeres typical for adult eumalacostracans, three additional vestigial segment anlagen occur in front of the telson. Furthermore, a true seventh pleonic ganglion and an eighth partial ganglion are formed embryologically. These fuse with the sixth pleonic ganglion anlage to form the terminal ganglion of the adult animal. I interpret these findings as recapitulations of ancestral characters, and they shed new light on the evolutionary transformation of crustacean segmentation patterns.
Material and Methods
The rearing and maintenance of embryos of the Australian freshwater crayfish Cherax destructor were described by Sandeman and Sandeman (1991). Their paper also defines the embryonic stages in percent of development and the postembryonic stages (e.g., PO I) that are used in the present investigation. Immunocytochemistry and fluorescent staining were described in detail in Scholtz et al. (1994) and Scholtz (1995).
A short summary of previous investigations
The cell lineage in the ectoderm of the germ band of Cherax was described in a previous study (Scholtz, 1992). As in most other malacostracans, the largest part of the germ band is formed by stem cells in the posterior growth zone, the ectoteloblasts. The ectoteloblasts produce transverse cell rows in an anterior direction by highly unequal divisions. Thirteen of these rows are formed (eI to eXIV) before the ectoteloblasts divide equally into the fourteenth and fifteenth rows (eXIV and eXV). Each row (eI to eXIV) cleaves twice, forming four regularly arranged descendant rows. The intersegmental furrow, separating two adjacent segments, is formed within the descendants of one original ectoderm row. In contrast to all other rows, row fifteen cleaves rapidly several times, forming a field of cells in a grid-like arrangement.
In Drosophila, the segment-polarity gene engrailed plays a crucial role in specifying the fate of the cells in the posterior part (compartment) of segments and in establishing the segmental boundaries (Lawrence, 1992). The expression pattern of engrailed is very similar in different insect and crustacean species. Therefore, a conserved function of the engrailed gene throughout the arthropods has been suggested (Patel, 1994). The basic modes of pleonic engrailed stripe formation described in the following correspond to those reported for other body regions of Cherax (Scholtz et al., 1993; Scholtz, 1995) and for other crustacean species (Patel et al., 1989; Scholtz et al., 1993, 1994). In the post-naupliar germ band of Cherax and other malacostracans, engrailed is expressed in the anterior descendants of each ectoderm row, and the intersegmental furrow is formed posterior to the engrailed stripes.
The formation of engrailed stripes
Nine engrailed stripes are formed in the embryonic pleon of C. destructor [ILLUSTRATION FOR FIGURE 1 OMITTED]. The first pleonic stripe appears in ectoderm row eIX and the sixth stripe in row eXIV. Stripes seven to nine are formed within the derivatives of row eXV.
The stripes appear in a strictly anteroposterior sequence [ILLUSTRATION FOR FIGURE 1 OMITTED]. At about 40% to 42% development the first engrailed stripe is formed and indicates the posterior margin of the prospective first pleomere [ILLUSTRATION FOR FIGURE 1A OMITTED]. The ninth pleonic engrailed stripe appears at about 65% development [ILLUSTRATION FOR FIGURES 1D, E OMITTED]. The formation of each individual stripe starts close to the midline and proceeds laterally [ILLUSTRATION FOR FIGURE 1D OMITTED]. The initial distance between the last two engrailed stripes of any stage is one row of engrailed negative cells. This is also true for stripes seven to nine [ILLUSTRATION FOR FIGURE 1E OMITTED]. Stripes one to seven are associated with the complex metamerically repeated cleavage pattern in the post-naupliar germ bands of Cherax. The cell division pattern in the area of stripes eight and nine, although not analyzed in detail, is somewhat different (Scholtz, 1992).
Initially, all stripes are one cell wide [ILLUSTRATION FOR FIGURE 1 OMITTED]. Also, at least pleonic stripes one to eight (not confirmed for pleonic stripe nine) pass through a transient widening phase caused by divisions of the engrailed-positive cells [ILLUSTRATION FOR FIGURES 1B, C OMITTED]. The widening phase is followed by narrowing to a one-cell width again due to the loss of engrailed expression in posterior cells in the stripe [ILLUSTRATION FOR FIGURES 1B, C OMITTED]. After narrowing, stripes one to seven widen during the morphogenesis of segmental structures such as intersegmental furrows, ganglia, and limb buds [ILLUSTRATION FOR FIGURE 1 OMITTED]. Stripes eight and nine disappear before widening takes place [ILLUSTRATION FOR FIGURE 1F OMITTED].
Stripes one to six surround the caudal papilla and form complete circles of about 40 engrailed-positive cells [ILLUSTRATION FOR FIGURE 1, 2A OMITTED]. Thus, engrailed is expressed in the midventral neurogenic region, in the lateral limb budding area, and in the dorsal portion of the forming segments one to six. Stripes seven to nine are restricted to the medioventral pan, which includes the neurogenic region [ILLUSTRATION FOR FIGURE 1D, E OMITTED]. They consist of seven to nine engrailed expressing cells.
Stripes one to seven show a twofold engrailed expression in the embryonic epidermis and in the forming ganglia [ILLUSTRATION FOR FIGURE 1, 2 OMITTED]. In the stages examined, the superficial epidermal engrailed expression continues in the forming limbs and the dorsal portions of the segments [ILLUSTRATION FOR FIGURE 2 OMITTED]. In the neurogenic area of advanced stages, engrailed expression is restricted to individual neuronal precursors and neurons, whereas the superficial engrailed expression has disappeared [ILLUSTRATION FOR FIGURE 1, 2 OMITTED]. In contrast to this, stripes eight and nine appear only transiently in the embryonic epidermis [ILLUSTRATION FOR FIGURE 1, 2 OMITTED].
In all other body regions, the intersegmental furrows are formed immediately posterior to the engrailed stripes [ILLUSTRATION FOR FIGURE 1 OMITTED]. This is also true for pleonic stripes one to six, but stripes seven to nine are not related to the formation of intersegmental furrows [ILLUSTRATION FOR FIGURE 1D, E, 2 OMITTED]. In segments one to six, limb buds are formed whose posterior portions are also engrailed positive [ILLUSTRATION FOR FIGURE 1, 2 OMITTED]. No limb buds occur in segments seven to nine, and in the corresponding regions the cells do not show engrailed expression [ILLUSTRATION FOR FIGURE 1, 2 OMITTED]. Interestingly enough, embryonic limb buds are formed in the first pleonic segment [ILLUSTRATION FOR FIGURE 1C, D OMITTED] where the adult C. destructor, like all parastacid crayfish species, is devoid of appendages in both sexes (Hobbs, 1988). The limbs associated with the sixth pleonic engrailed stripe are clearly the posteriormost appendages on the germ band [ILLUSTRATION FOR FIGURE 1C, D, E, 2 OMITTED]. On the basis of their shape in advanced developmental stages, they can be identified to be the uropods [ILLUSTRATION FOR FIGURE 1, 2 OMITTED].
In the pleonic segments one to seven, engrailed is expressed in cells of the forming ganglia [ILLUSTRATION FOR FIGURE 1, 2 OMITTED]. Thereby, the arrangement of engrailed-positive cells (neurons ?) is very similar between the seventh and more anterior segments [ILLUSTRATION FOR FIGURE 2 OMITTED]. The engrailed expression in stripes eight and nine disappears at about 70% to 75% development and is not correlated with neurogenesis. The staining of the embryonic central nervous system with rhodamine-labeled phalloidin reveals that a true seventh embryonic ganglion is formed in addition to the anterior six pleonic ganglion anlagen [ILLUSTRATION FOR FIGURE 3 OMITTED]. All pleonic ganglion anlagen one to seven share the occurrence of two main commissures and a characteristic median Y-shaped neuron that might correspond to the neuron S described by Whiting-ton et al. (1993) [ILLUSTRATION FOR FIGURE 3A, B OMITTED]. Posterior to the seventh, an eighth ganglion anlage is formed. It possesses only one commissure, and the characteristic median cell is lacking [ILLUSTRATION FOR FIGURE 3B OMITTED]. Furthermore, no neuronal engrailed expression occurs. From this eighth hemiganglion, two nerves run posteriorly towards the embryonic telson region [ILLUSTRATION FOR FIGURE 3B OMITTED]. During further ontogenesis the anlagen of ganglia six, seven, and eight fuse and become a morphological unit that forms the terminal ganglion of the adult animals [ILLUSTRATION FOR FIGURE 3C OMITTED]. Thereby the commissures remain separated. The coalescence of these ganglion anlagen is clearly visible from about 80% development. However, engrailed expression still indicates the composed origin of the terminal ganglion in postembryonic stages (e.g., PO I) [ILLUSTRATION FOR FIGURE 4 OMITTED].
Development of the terminal ganglion
The present investigation shows that the terminal ganglion of the adult parastacoid crayfish Cherax destructor is the fusion product of three embryonic ganglion anlagen - the sixth and seventh pleonic ganglia and a partial eighth ganglion. This developmental pattern corresponds to that described for the asiacold crayfish Procambarus clarkii (Dumont and Wine, 1987). Furthermore, these embryological data are consistent with results from neuroanatomical and immunohistochemical studies analyzing the terminal ganglia of the adults of several freshwater crayfish species (Stoll, 1925; Kondoh and Hisada, 1986; Audehn et al., 1993) and of the lobster Homarus gammarus (Winlow and Laverack, 1972). The embryonic morphology and the pattern of engrailed expression of the seventh pleonic ganglion resemble to a high degree those of the anterior pleonic ganglia. This suggests that it represents a true segmental ganglion homologous with the anterior segmental ganglia. The eighth pleonic ganglion anlage shows only one commissure. Furthermore, this ganglion lacks any engrailed expression which characterizes the posterior part of forming ganglia, although an epidermal eighth pleonic engrailed stripe is formed. Taken together, this suggests that the eighth pleonic ganglion of the embryo might be the anterior part of a true segmental ganglion anlage. On the basis of the occurrence of specifically arranged identified neurons, Audehn et al. (1993) came to similar conclusions.
The formation of an embryonic anlage of a seventh pleonic ganglion that later fuses with the sixth ganglion has been reported from representatives of most highermalacostracan taxa including Leptostraca (Claus, 1888; Manton, 1928b, 1934), Hoplocarida (Shiino, 1942), Syncarida (Hickman, 1937), Mysidacea (Manton, 1928a, b), Tanaidacea (Scholl, 1963), and Isopoda (Stromberg, 1967). No seventh pleonic ganglion occurs in the embryo of the amphipod Gammarus pulex; however, for a short time during development, the anlage of the sixth pleonic ganglion is subdivided into two distinct adjacent areas - a phenomenon interpreted as a vestigial formation of a seventh pleonic ganglion (Weygoldt, 1958). None of these authors has mentioned the partial eighth pleonic ganglion, but this might be due to the techniques used (no whole-mounts or horizontal sections). Adult eumalacostracans possess only six pleonic ganglia (see Hanstrom, 1928), and this is also true for leptostracans with a seventh pleomere (Claus, 1888; Manton, 1928a). Against this background, I conclude that the composite nature of the terminal (sixth) ganglion and the pattern of its formation by fusion during embryogenesis is part of the malacostracan ground plan. Thus, the fusion of the terminal ganglion is apparently not correlated with the evolution of the uropods and their complex function in eumalacostracans.
Origination of the uropods from the sixth pleomere
The anterior six engrailed stripes in the embryonic pieon of Cherax mark the posterior border of the six pleomeres that persist in the adult. Engrailed is expressed in the ventral region comprising the ganglion primordia and the limb buds as well as the lateral and dorsal sides of each segment. The seventh to ninth pleonic engrailed stripes are restricted to the ventral side of the embryo. However, from the mode of formation and the distance between them, they correspond to the anterior stripes. Thus I conclude that all pleonic engrailed stripes are serial homologues and that stripes seven to nine also indicate segment anlagen.
The pattern of the sixth engrailed stripe clearly reveals that the uropods of Cherax are the limbs of the sixth pleomere, which is also true for the mysid Neomysis integer (unpub. obs.). This result confirms some of the suggestions of Manton (1928a, b), and since there is good evidence that the tail fans of all eumalacostracan groups are homologous (Hessler, 1983; Wagele, 1994), the findings presented here might also be valid for eumalacostracans in general. Therefore, Siewing's (1956, 1963) hypothesis that the uropods originate from the seventh pleon segment cannot be maintained. The present results also contradict the assumption that the caudal rami of the telson of leptostracans are homologous with the eumalacostracan uropods (Bowman, 1971: for further arguments against this view see Schminke, 1976). Furthermore, the telson of decapods does not correspond to the ancestral seventh pleomere, as was suggested by Kondoh and Hisada (1986).
The additional engrailed stripes seven to nine lie clearly in front of the telson anlage, which is characterized by the proctodeum and which lacks engrailed expression. Against this background, the seemingly "seven-segmented" pleon with uropods originating from the "seventh" pleomere of some lophogastrids is not plesiomorphic, as considered by Manton (1928b), Siewing (1956), and Lauterbach (1975), but is a derived feature. There is ontogenetic and phylogenetic evidence for this suggestion. Manton's (1928b) hypothesis that the uropods migrate posteriorly before the border between the last two segments is formed is not consistent with the finding that the intersegmental furrows are formed before limb buds appear (Scholtz, 1990; present investigation). We know from Drosophila genetics that the establishment of the segmental border is the prerequisite for the subsequent differentiation of segments (Lawrence, 1992). Therefore, the "seventh pleonic segment" of lophogastrids is apparently the result of a secondary nonsegmental(?) subdivision of the terminal eumalacostracan segment, as was suggested earlier by Claus (1888). With respect to the position of lophogastrids in the eumalacostracan phylogenetic tree (e.g. Siewing, 1956; Richter, 1993), it is more likely that a subdivision of the terminal segment occurred only once in the lophogastrid line than that the seventh pleomere has been lost independently in several eumalacostracan lines.
The seventh pleonic engrailed stripe in the embryo of Cherax is an obvious example of the recapitulation of ancestral conditions (see Sudhaus and Rehfeld, 1992). It demarcates the posterior border of an additional (seventh) pleonic segment that is missing in adult crayfish and other eumalacostracans but is present in adult Leptostraca. the sister-group of the Eumalacostraca. There is no reason to assume that pedomorphosis led to the occurrence of the seventh segment in adult leptostracans and to the loss of the highly complex eumalacostracan tail-fan (Hessler, 1983; Paul et al., 1985) in this group.
Interestingly, in the crayfish as in other eumalacostracans, the corresponding seventh pleonic ganglion persists and is fused with the sixth to form a morphological and functional unit (see above). In addition, some authors report that the embryos of several malacostracan species contain terminal mesodermal somites that might be related to a vestigial seventh pleonic segment and that also fuse with the sixth pleonic somites (e.g., Manton, 1928a; Shiino, 1942). Those processes can be characterized as fusions, but fusion does not seem to be the appropriate description for events in the superficial segmental parts. The pleonic engrailed stripe seven (like stripes eight and nine) is more like a transient segment anlage that is not involved in morphogenesis and that disappears during further development. From the outset, the morphological border between the terminal segment and the telson lies behind the sixth pleonic engrailed stripe.
Phylogenetic significance of pleonic engrailed stripes eight and nine
The eighth and ninth pleonic engrailed stripes are also considered to indicate vestigial segments that recapitulate ancestral conditions. This suggestion is based on the similar appearance of stripes seven to nine and on the fact that many non-malacostracan crustaceans possess more segments than malacostracans. However, it is difficult to say how far back stripes eight and nine point in phylogeny and in which ancestral lineage these segments have been lost in the adults. The question of whether segmentation and tagmatization of the Malacostraca are primitive or are derived within the Crustacea has been debated, and the many attempts to reconstruct the crustacean stem species have yielded very different results concerning tagmosis and segment number. The proposals reach from short animals with only a few segments (Muller, 1864) to forms with many segments (Hessler and Newman, 1975; Lauterbach, 1986), and from forms with a more or less homonomously segmented trunk (Hessler and Newman, 1975; Schram, 1982; Walossek, 1993) to animals with a distinct subdivision of the trunk into thorax and a limbless abdomen (Lauterbach, 1986; Fryer, 1992). But until the phylogenetic relationships between the higher crustacean taxa are resolved - see Siewing (1963), Schram (1986), and Wilson (1992) for various proposals - the reconstruction of a crustacean ground plan (sensu Hennig, 1966) will be pure speculation.
Nevertheless, the present findings permit some tentative conclusions. The occurrence of additional segment remnants in the embryonic pleon of Cherax argues against an original number of 15 trunk segments in crustaceans or even mandibulates as suggested by Walossek (1993); the number of trunk segments in the crustacean stem species must have been higher. Therefore, the additional engrailed stripes in the pleon of Cherax rather argue in favor of Lauterbach's (1975) hypothesis of a loss of posterior segments in the ancestral lineage of malacostracans. The restriction of these additional stripes to the neural region and the entire lack of limb anlagen furthermore support the suggestion that these segments are vestiges of the limbless abdomen postulated by Lauterbach (1986) and Fryer (1992) for the crustacean stem species.
I thank David Sandeman and Renate Sandeman for their helpful advice as well as for the opportunity to use their crayfish culture and to work in their laboratory. The anti-engrailed antibody was a generous gift from Nipam Patel. I am grateful to Stefan Richter, Wolfgang Dohle, and David Sandeman for critically reading the manuscript. This work was supported by grants from the University of New South Wales (Visiting Fellowship) and from the Deutsche Forschungsgemeinschaft (Scho 443/3-1).
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|Date:||Apr 1, 1995|
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