Integrative and Comparative Biology Advance Access originally published online on February 16, 2006
Integrative and Comparative Biology 2006 46(2):195-206; doi:10.1093/icb/icj020
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Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships
Department of Zoology, University of Cambridge Downing Street, Cambridge CB2 3EJ, UK
Correspondence: 1E-mail: stollewe{at}uni-mainz.de
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Synopsis
IntroductionSeveral alternative hypotheses on the relationships between the major arthropod groups are still being discussed. We reexamine here the chelicerate/myriapod relationship by comparing previously published morphological data on neurogenesis in the euarthropod groups and presenting data on an additional myriapod (Strigamia maritima). Although there are differences in the formation of neural precursors, most euarthropod species analyzed generate about 30 single neural precursors (insects/crustaceans) or precursor groups (chelicerates/myriapods) per hemisegment that are arranged in a regular pattern. The genetic network involved in recruitment and specification of neural precursors seems to be conserved among euarthropods. Furthermore, we show here that neural precursor identity seems to be achieved in a similar way. Besides these conserved features we found 2 characters that distinguish insects/crustaceans from myriapods/chelicerates. First, in insects and crustaceans the neuroectoderm gives rise to epidermal and neural cells, whereas in chelicerates and myriapods the central area of the neuroectoderm exclusively generates neural cells. Second, neural cells arise by stem-cell-like divisions of neuroblasts in insects and crustaceans, whereas groups of mainly postmitotic neural precursors are recruited for the neural fate in chelicerates and myriapods. We discuss whether these characteristics represent a sympleisiomorphy of myriapods and chelicerates that has been lost in the more derived Pancrustacea or whether these characteristics are a synapomorphy of myriapods and chelicerates, providing the first morphological support for the Myriochelata group.
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Introduction |
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The relationships between and within the major arthropod groups have not been consistently resolved. Several alternative hypotheses are being discussed. The so-called Mandibulata hypothesis suggests a clade composed of insects, crustaceans, and myriapods with various ideas as to the relationships within this clade. The Pancrustacea hypothesis assumes a crustacean origin of insects or a sister group relationship between both groups (Zrzav
and 
tys 1997
; Shultz and Regier 2000; Dohle 2001; Mallatt and others 2004; Regier and others 2005), and the Atelocerata hypothesis unites insects and myriapods as a clade (Snodgrass 1938, 1950, 1951; Briggs and Fortey 1989; Schram and Emerson 1991; Bergström 1992; Wheeler WC and others 1993; Kraus O and Kraus M 1994, 1996; Emerson and Schram 1998; Wheeler WC 1998; Wills and others 1998; Bitsch C and Bitsch J 2004). Whereas the Atelocerata hypothesis is mainly supported by morphological evidence, the idea of Pancrustacea was initially based on the phylogenetic analysis of ribosomal-RNA sequence data in which crustaceans and insects grouped together to the exclusion of myriapods (Field and others 1988; Turberville and others 1991; Ballard and others 1992; Friedrich and Tautz 1995; Giribet and Ribera 1998). Recent data on comparative developmental biology support this molecular sister group relationship, although the synapomorphies seem to be shared mainly by insects and malacostracans (Dohle and Scholtz 1988; Patel and others 1989; Whitington and others 1993; Osorio and others 1995; Whitington 1996; Dohle 1998; Nilsson and Osorio 1998; Duman-Scheel and Patel 1999; Dohle 2001). Several independent phylogenetic analyses based on molecular data support a chelicerate/myriapod sister group relationship, the so-called Myriochelata hypothesis (Friedrich and Tautz 1995; Hwang and others 2001; Kusche and Burmester 2001; Nardi and others 2003; Mallatt and others 2004; Pisani and others 2004), a link that had never been considered by comparison of morphological structures. However, recent comparative studies on neurogenesis in the diplopod Glomeris marginata and the chilopod Lithobius forficatus have shown that the myriapods and the chelicerates share several features that cannot be found in homologous form in insects and crustaceans. The most distinctive difference is that groups of neural precursors are singled out from the neuroectoderm of the spider and the myriapods, rather than individual cells (that is, neuroblasts) as in insects or crustaceans (Fig. 1) (Cupiennius salei: Stollewerk and others 2001; Limulus polyphemus: Mittmann 2002; C. salei: Stollewerk 2002; Stollewerk and others 2003; G. marginata: Dove and Stollewerk 2003; L. forficatus: Kadner and Stollewerk 2004).
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Here we give an overview of the modes of neurogenesis in the major arthropod groups with special focus on myriapods and chelicerates. Furthermore, we present new data on the geophilomorph centipede Strigamia maritima (Myriapoda) and discuss the data in a phylogenetic context.
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Neural precursor formation in insects |
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Neurogenesis has been studied in detail in the insect Drosophila melanogaster. The ventral neuroectoderm of the Drosophila embryo gives rise to both neural and ectodermal cells (Jiménez and Campos-Ortega 1979
, 1990; Cabrera and others 1987). The competence to adopt the neural fate depends on the presence of the proneural genes achaete, scute, and lethal of scute. These genes are expressed in clusters of cells in each hemisegment at the beginning of neurogenesis. In a second step, proneural gene expression is restricted to a single cell of the cluster, the future neuroblast (Cabrera and others 1987; Romani and others 1987; Skeath and others 1992). This process is called lateral inhibition and is mediated by the neurogenic genes Notch and Delta (Simpson 1990; Martin-Bermudo and others 1995; Heitzler and others 1996; Seugnet and others 1997). It has been predicted that proneural gene expression is higher in a particular cell of the proneural cluster as a result of predetermination or an extrinsic signal. Since the proneural genes activate the expression of Delta, Delta is also up-regulated in this cell. Delta binds to Notch and activates Notch in the neighboring cells, which eventually leads to the activation of the E(spl) genes. The gene products of this complex repress proneural gene expression, which in turn leads to a down-regulation of Delta in neighboring cells (Nakao and Campos-Ortega 1996; Ligoxygakis and others 1998). As a result of this feedback loop, proneural gene expression is maintained in the neuroblast but down-regulated in the remaining cells of the proneural cluster. Although this model predicts a higher expression of Delta in single cells (presumptive neuroblasts), it has not been demonstrated that Delta transcripts accumulate at higher levels in individual cells within the proneural clusters. Once a neuroblast is determined, it delaminates into the embryo and divides asymmetrically to produce ganglion mother cells (Goodman and Doe 1993). The ganglion mother cells divide only once to give rise to neural cells that differentiate into neurons and glia. The neuroblasts do not delaminate all at once but in 5 discrete waves. Each neuroblast has a distinct identity and gives rise to an invariant lineage of neural progenies. The identity of the neuroblasts is specified in the ventral neuroectoderm by segment polarity and dorsoventral patterning genes (see review in Skeath 1999).
Neurogenesis has also been studied in insects other than Drosophila. The pattern of neuroblasts is similar in all insects analyzed: they are arranged in 7 anteroposterior rows with 3–6 neuroblasts each (Bate 1976; Broadus and Doe 1995; Wheeler SR and others 2003). It has been shown in Tribolium castaneum and in Schistocerca americana that single neuroblasts are selected in sequential waves, similar to D. melanogaster (Broadus and Doe 1995; Wheeler SR and others 2003). Within the insect group, proneural genes have been identified in several Diptera, a butterfly, and the flour beetle T. castaneum (Precis coenia: Galant and others 1998; Ceratitis capitata: Wülbeck and Simpson 2000; Calliphora vicina: Pistillo and others 2002; Phormia terranovae: Skaer and others 2002; Anopheles gambiae: Wülbeck and Simpson 2002; T. castaneum: Wheeler SR and others 2003).
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Neural precursor formation in malacostracan crustaceans |
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Neuroblasts have also been described in malacostracan crustaceans and exist perhaps also in branchiopods (Leptochelia spp.: Dohle 1972
; Diastylis rathkei: Dohle 1976; Neomysis integer: Scholtz 1984; Peracarida: Dohle and Scholtz 1988; Gammarus pulex: Scholtz 1990; Cherax destructor: Scholtz 1992; Leptodora kindti: Gerberding 1997; Decapoda: Harzsch and others 1998; Harzsch 2001; Scholtz and Gerberding 2002; Harzsch 2003). However, there are several differences from insect neuroblasts. Neuroblasts in malacostracan crustaceans are generated by so-called ectoteloblasts, specialized stem cells that are located in the posterior region of the germ band anterior to the proctodeum (with the exception of Amphipoda; Scholtz 1990). Furthermore, crustacean neuroblasts do not delaminate into the embryo but remain in the outer surface. Similar to insects, crustacean neuroblasts divide asymmetrically to give rise to smaller ganglion mother cells that are pushed into the embryo by directed mitosis (Scholtz 1992). The ganglion mother cells also divide once to produce 2 neurons. In contrast to insects, crustacean neuroblasts can generate epidermal cells after budding off ganglion mother cells (Scholtz and Gerberding 2002). Two achaete-scute homologues have been identified in the branchiopod crustacean Triops longicaudatus (Wheeler SR and Skeath 2005). The expression pattern of these genes is similar to the distribution of transcripts of the Achaete-Scute Complex genes in Drosophila. |
Neural precursor formation in chelicerates and myriapods |
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In a few classical accounts, neuroblasts have been described in 3 chelicerate species, but it is possible that the data were partly misinterpreted owing to technical limitations at the time (Yoshikura 1955
; Mathew 1956; Winter 1980). Apart from these studies, the literature suggests that neurogenesis occurs by a generalized inward proliferation of neuroectodermal cells to produce paired segmental thickenings in chelicerates and myriapods (Anderson 1973). However, recent analyses of neurogenesis in 2 chelicerates (both spiders) and 2 myriapods (a diplopod and a chilopod) have revealed that in contrast to insects and crustaceans, groups of neural precursors are specified for neural fate (Fig. 1) in both myriapods and chelicerates (Stollewerk and others 2001; Mittmann 2002; Stollewerk 2002; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). Although the neural precursors arise in 4 sequential waves in regions that are prefigured by proneural genes, similar to Drosophila, the precursor groups form invagination sites that persist in the ventral neuroectoderm during the entire course of neurogenesis. Approximately 30 invagination groups per hemisegment detach from the apical surface at about the same time, 3 days after the beginning of neurogenesis. Interestingly, the invagination groups show a similar pattern in the myriapods and the spider (Fig. 2): they are arranged in 7 transverse rows with 3–6 invagination sites each (Stollewerk and others 2001; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). Although the final pattern of invagination sites is similar in both groups (Fig. 2), the order of formation of the individual invagination groups is different. In both the spider C. salei and the chilopod L. forficatus, the first invagination sites arise in the anteriolateral region of each hemisegment, whereas in the diplopod G. marginata, the first invaginating groups are visible in the middle of each hemisegment (Stollewerk and others 2001; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). One can be speculate that this difference in timing has an impact on the identity of the neural precursors in Glomeris compared with the spider and the chilopod, as genes that are involved in neural diversity might be expressed during different time windows in the ventral neuroectoderm.
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To obtain more data on diverse myriapod groups, we analyzed neurogenesis in the geophilomorph centipede S. maritima. In contrast to Lithobius and Glomeris, Strigamia undergoes so-called epimorphic development. Myriapods showing this kind of development generate all segments during embryogenesis, whereas in Lithobius and Glomeris further segments are added during posthatching larval stages. Since Strigamia does not have a considerably longer period of embryogenesis (approximately 30 days [Arthur and Chipman 2005
], compared with approximately 15 days in Cupiennius, Lithobius, and Glomeris), the 50 or so segments must arise and differentiate in quick succession. This raises the question of whether neural precursor formation is altered in adaptation to an accelerated development of individual segments.
In Strigamia segments arise from a posterior undifferentiated disc (Chipman and others 2004b). As segments are added sequentially, the older segments begin to differentiate, with the first signs of neurogenesis becoming apparent approximately 5–6 segments anterior to the undifferentiated area that is the fifth or sixth youngest segment (Chipman and Stollewerk 2006). As the segments arise from the posterior disc, they are broad in their mediolateral extent and anteroposteriorly compressed (Fig. 3A and B). Shortly after their first appearance, they separate into clear left and right hemisegments. Morphogenetic movements cause individual segments to broaden along the anteroposterior axis while the mediolateral extent is reduced (Fig. 3C). Later in development, after all of the segments have been generated, the left and right halves of the germ band drift apart in a process known as lateral migration (Kettle and others 2003; Chipman and others 2004b). Throughout development, there is an anterior to posterior gradient in the degree of differentiation of individual segments, spanning a wide range of stages in the neurogenic process. This allows the whole course of neurogenesis to be observed in a small number of specimens.
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Similar to the spider and the other myriapods, Strigamia has approximately 30 invagination sites per hemisegment (based on counts of invagination sites at different axial positions in multiple embryos). In the narrow posterior segments, they arise at stereotypical positions (see below) and are eventually arranged in 3 rows (Fig. 3B). Interestingly, the morphogenetic movements that reduce the mediolateral extent of the segments lead to an arrangement of the invagination sites that is similar to the other myriapods and the spider: they are arranged in 7 rows with 3–6 invagination sites each (Fig. 3C; compare with Glomeris Fig. 3D).
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Proneural genes in the spider and the myriapods |
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In Drosophila the proneural genes are essential for neural fate. The genes of the so-called Achaete-Scute Complex achaete, scute, and lethal of scute are expressed prior to formation of the neuroblasts in the ventral neuroectoderm (Jiménez and Campos-Ortega 1979
, 1990; Cabrera and others 1987; Martin-Bermudo and others 1991). Mutations in these genes lead to the absence of neuroblasts. Homologues of achaete-scute have been identified in the spider C. salei and the myriapods G. marginata and L. forficatus (Stollewerk and others 2001; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). As in Drosophila, these homologues can be detected in regions of the neuroectoderm where neural precursors will be generated hours later. Expression is up-regulated in the neural precursor groups, and transcription is down-regulated in the surrounding cells. This expression pattern is different from that in Drosophila, where proneural transcripts become restricted to single cells (neuroblasts). Functional studies in the spider have shown that the achaete-scute homologues are essential for neural fate, similar to the case of Drosophila (Stollewerk and others 2001). |
Neurogenic genes in the spider and the myriapods |
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It has been shown in Drosophila that the neurogenic genes Notch and Delta are responsible for the restriction of proneural gene expression to a single cell of a cluster (Simpson 1990
; Martin-Bermudo and others 1995; Heitzler and others 1996; Seugnet and others 1997). However, a dynamic expression of Delta (mRNA and protein) that correlates with the specification of neuroblasts has not been observed in the central nervous system of fly embryos, although it is assumed that within a proneural cluster the cell expressing the highest level of Delta is selected for the neural fate. Similarly, Notch seems to be expressed at homogeneous levels in all ventral neuroectodermal cells, indicating that Notch transcripts are not excluded from neural precursors (Heitzler and Simpson 1993).
Two Delta homologues, CsDelta1 and CsDelta2, have been identified in the spider C. salei, and 1 Delta homologue each in the myriapods G. marginata and L. forficatus (Stollewerk 2002; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). In contrast to the case of flies, expression of the spider CsDelta2 and the myriapod Delta genes can be correlated with the formation of neural precursors. Delta transcripts can be detected in all neuroectodermal cells but accumulate in the invaginating neural precursors. Furthermore, the spider and myriapod Notch homologues (1 in each species) show a heterogeneous expression pattern throughout neurogenesis. The up-regulation of Notch in distinct regions in the spider and the myriapods might correlate with the formation of invagination sites, but this has to be analyzed in more detail. Functional studies in the spider revealed that Notch and Delta mediate lateral inhibition, similar to the case of Drosophila, although groups of neural precursors, rather than single cells, are selected.
We have identified 1 Delta and 1 Notch homologue in S. maritima (Chipman and Stollewerk 2006). StmNotch shows a heterogeneous expression pattern similar to the spider and the other myriapods (data not shown). However, the expression pattern of the Strigamia Delta gene is different from that in the other euarthropod groups (Fig. 4). First, Delta expression reveals that invagination sites are added continuously during neurogenesis. In the most posterior segment of the Strigamia embryo that exhibits neurogenesis (representing the earliest stages of neurogenesis), 2 invagination sites are visible (Fig. 4A). In the next anterior (developmentally older) segment, an additional invagination site has been generated, and in the next anterior segment a further 2 invagination sites have been added. This pattern suggests that invagination sites are added continuously during neurogenesis, rather than in several distinct waves as in the spider and the other myriapods.
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Furthermore, StmDelta transcripts seem to accumulate at higher levels in single cells within the invagination groups (arrows in Fig. 4B and C). The single cells are surrounded by cells expressing lower levels of Delta (Fig. 4). To understand this expression pattern, we further analyzed the morphology of the invaginating cell groups by staining Strigamia embryos with phalloidin-FITC, a dye that stains the actin cytoskeleton. An accumulation of actin around single cells in the ventral neuroectoderm was observed by confocal microscopy (Fig. 5A). A detailed analysis of the morphology of the invagination groups revealed that this staining is due to the cell processes of the cells of individual invagination groups that are attached to a single cell of the group (Fig. 5B and C). These data suggest that StmDelta transcripts are not present at higher levels in single cells but accumulate around single cells within invagination groups as a result of this distinct morphological arrangement.
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Specification of neuroblast identity in arthropods |
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In Drosophila, segment polarity genes and dorsoventral patterning genes are expressed during neurogenesis in the ventral neuroectoderm (see review in Skeath 1999
). These genes subdivide the neuroectoderm into a gridlike pattern, so that each proneural cluster shows a different gene expression profile. The neuroblasts maintain the specific expression pattern of the proneural cluster from which they delaminate and give rise to an invariant lineage of distinct neural progenies. Thirty neuroblasts delaminate from the neuroectoderm of each hemisegment. They are arranged in 7 rows with each row expressing a different subset of segment polarity genes. It has been shown in Drosophila that the function of the segment polarity genes is specifically required in neuroblasts. Mutations in these genes lead either to the absence of specific neuroblasts or to changes in the identity of neuroblasts (Skeath 1999).
The specification of neuroblast identity has not been analyzed in any detail in arthropods other than Drosophila. Although segment polarity genes have been identified in other insects, in crustaceans, in myriapods, and in a spider, their function during neurogenesis has not been studied except for engrailed (Patel and others 1992; Brown and others 1994, 1997; Dawes and others 1994; Patel 1994; Damen and others 2000; Telford 2000; Davis and others 2001; Damen 2002; Dearden and others 2002; Hughes and Kaufman 2002; Mouchel-Vielh and others 2002; Copf and others 2003; Kettle and others 2003; Chipman and others 2004a, 2004b; Eckert and others 2004; Janssen and others 2004; Peel 2004). However, Patel and coworkers (1989) investigated the expression pattern of the segment polarity gene engrailed in several insects and crustaceans and showed that engrailed expression in neuroblasts is conserved. In all species analyzed, engrailed is expressed in neuroblast rows 6 and 7, and 1 neuroblast of row 1.
We have analyzed engrailed expression in the spider Cupiennius and the geophilomorph centipede Strigamia. In both the spider and the centipede, engrailed is expressed in segmental stripes in the posterior region of the germ band (Fig. 6A and D) (Damen 2002; Kettle and others 2003; Chipman and others 2004b). In more anterior, developmentally advanced segments that are undergoing neurogenesis, engrailed expression covers a broader region at the posterior border of the segments. In addition, in the central area of the ventral neuroectoderm the engrailed expression domain extends into the anterior region of the next posterior segments, whereas the engrailed stripe lateral to the limb buds is still restricted to a few cell rows at the posterior border of the segments (Fig. 6A and B, arrows; Fig. 7A; Damen 2002). In spiders and myriapods, all cells of the ventral neuroectoderm give rise to neural cells. The epidermis arises lateral to the neuromeres only after invagination of the neural precursors (Stollewerk 2002; Dove and Stollewerk 2003; Stollewerk 2004). Therefore, it can be concluded that during neurogenesis, engrailed is specifically expressed in neural precursors.
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In Strigamia, engrailed is expressed in the ventral midline (Fig. 6B). Further analysis will show whether this expression corresponds to an accumulation of transcripts in neural cells.
We have compared the pattern of engrailed expression with the pattern of invagination sites in the spider. Single-color double-staining with engrailed and anti-horseradish peroxidase, which is exclusively expressed in the cell processes of the invaginating neural precursor groups at this time, revealed that engrailed is expressed in the invagination groups of rows 6 and 7 and row 1 in the spider (Fig. 7A–D). Interestingly, there are 7 invagination sites in rows 6 and 7 and this number is identical to the number of neuroblasts that are engrailed positive in rows 6 and 7 in insects and crustaceans (Patel and others 1989; Duman-Scheel and Patel 1999).
We have also compared engrailed expression with the position of invagination sites in the geophilomorph centipede. In Strigamia the segments have a peak and trough structure that is most obvious in sagittal sections (Figs. 6D and 8D). In the posterior region of the germ band the engrailed stripe divides the trough into 2 halves (Fig. 6D). Based on this expression pattern and the fact that the posterior border of the engrailed domain coincides with the posterior border of segments in all arthropods analyzed, we conclude that the posterior half of the trough belongs to the next posterior segment. In more anterior segments that exhibit neurogenesis, engrailed is expressed throughout the trough, indicating that it is not only expressed at the posterior border of the segments but also in neural precursors in the anterior region of each segment. Analysis of phalloidin-FITC-stained embryos revealed that the neural precursor groups that belong to the anterior row of invagination sites extend into the groove (Fig. 8B and C). Similarly, the groups that belong to the posterior rows extend into the groove from the other site (Fig. 8B). Double-stainings with Delta and engrailed suggest that engrailed is expressed in the first anterior row of invagination groups and both in rows 6 and 7 (Fig. 8E).
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Conclusions |
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We have presented comparative morphological and molecular data on neurogenesis in the euarthropod groups. Although there are differences in the formation of neural precursors, most arthropod species analyzed generate approximately 30 single neural precursors (insects/crustaceans) or precursor groups (chelicerates/myriapods) per hemisegment, which are arranged in regular rows. Homologues of achaete-scute are necessary for the formation of neural precursors, and the neurogenic genes Notch and Delta restrict the proportion of cells that adopt a neural fate at a certain time. In insects, chelicerates, and 2 of the 3 myriapods analyzed, neural precursors are produced in several sequential waves. Neural precursor formation has been analyzed in only a limited number of crustacean species (Dohle 1972
, 1976; Scholtz 1984, 1990, 1992; Harzsch and Dawirs 1994, 1996; Harzsch and others 1998; Gerberding and Scholtz 1999; Harzsch 2001, 2003). Based on the small amount of data available, it can be assumed that neuroblasts in crustaceans are continuously added during neurogenesis, rather than being generated in several waves. The continuous addition of neural precursor groups in the centipede Strigamia might be an adaptation to the distinct embryonic development of this species. Approximately 50 segments are generated during embryogenesis and differentiate in quick succession. Gene expression studies and morphological analyses revealed that each segment exhibits a different differentiation state along the anterior-posterior axis during neurogenesis. Therefore, it can be concluded that each segment initiates neurogenesis on its own, rather than being synchronized with several segments, as seen in the spider and in the other myriapods. As has been shown previously, neurogenesis occurs simultaneously in the prosoma of the spider and in the head and first trunk segments of G. marginata and L. forficatus, and at least 2 to 3 segments show the same stage of neurogenesis in the posterior region of the germ band (Stollewerk and others 2001; Dove and Stollewerk 2003; Kadner and Stollewerk 2004). Despite the differences in neural precursor formation in the euarthropod group, neural precursor identity seems to be achieved in a similar way. In all species analyzed, engrailed is expressed in neural precursor rows 6, 7, and 1.
In addition to these conserved features, we found 2 characteristics that distinguish insects/crustaceans from myriapods/chelicerates. First, in insects and crustaceans the neuroectoderm gives rise to epidermal and neural cells. In contrast, there is no decision between epidermal and neural fate in the central region of the ventral neuroectoderm of chelicerates and myriapods. The epidermis arises lateral to the neuromeres and overgrows the ventral nerve cord after formation of neural precursors. However, this characteristic seems to be ancestral (plesiomorphic), as it has been shown in onychophorans (a group that is assumed to be basal to the arthropods) that the whole central regions of the hemisegments sink into the embryo and thus give only rise to neural cells (Eriksson and others 2003). The second distinguishing characteristic is the presence of neuroblasts in insects/crustaceans as opposed to neural precursor groups in myriapods/chelicerates. Invaginating cell groups have not been found in onychophorans or in tardigrades (another potential outgroup to the euarthropods (Eriksson and others 2003; Hejnol and Schnabel 2005). However, only 2 species have been analyzed, which might be derived and thus do not represent the ancestral state. The fact that approximately 30 neural precursors/precursor groups per hemisegment are arranged in a strikingly similar pattern in most euarthropod species analyzed suggests that a similar pattern was present in the last common ancestor of the arthropods. The formation of neural precursor groups could be a sympleisiomorphy of myriapods and chelicerates that has been lost in the more derived Pancrustacea. However, it is also possible that this characteristic represents a synapomorphy of myriapods and chelicerates, providing the first morphological support for the Myriochelata group (Friedrich and Tautz 1995; Hwang and others 2001; Kusche and Burmester 2001; Nardi and others 2003; Mallatt and others 2004; Pisani and others 2004). At present, we cannot distinguish between these 2 scenarios, but the data presented in this review are clearly inconsistent with the Atelocerata hypothesis, which unites myriapods and insects, to the exclusion of crustaceans. These data are intriguing and warrant further research into neurogenesis in putative arthropod sister groups. Additional data will allow a polarization of the characteristic state changes and help resolve the question of the relationships between the major arthropod groups.
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Acknowledgements |
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We thank the organizers of the symposium for the opportunity to present our work. We are grateful to Michael Akam and Pat Simpson for providing lab space and for helpful discussions. Thanks to Pat Simpson for critical reading of the manuscript. The Deutsche Forschungsgemeinschaft (A.S.) and Federation of European Biochemical Societies (A.D.C.) supported this research.
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Footnotes |
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2Present address: Johannes-Gutenberg University Mainz, Department of Genetics, Johann-Joachim-Becherweg 32, 55099 Mainz, Germany.
From the symposium "The New Microscopy: Toward a Phylogenetic Synthesis" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, at San Diego, California.
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