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Neurogenesis in Myriapods and Chelicerates and Its Importance for Understanding Arthropod Relationships Angelika Stollewerk1,2 and Ariel D

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Neurogenesis in Myriapods and Chelicerates and Its Importance for Understanding Arthropod Relationships Angelika Stollewerk1,2 and Ariel D 195 Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships Angelika Stollewerk1,2 and Ariel D. Chipman Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK Synopsis Several 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 neuro- genesis 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. Introduction myriapods (Field and others 1988; Turberville and The relationships between and within the major others 1991; Ballard and others 1992; Friedrich and arthropod groups have not been consistently resolved. Tautz 1995; Giribet and Ribera 1998). Recent data Several alternative hypotheses are being discussed. on comparative developmental biology support this The so-called Mandibulata hypothesis suggests a molecular sister group relationship, although the clade composed of insects, crustaceans, and myriapods synapomorphies seem to be shared mainly by insects with various ideas as to the relationships within this and malacostracans (Dohle and Scholtz 1988; Patel and clade. The Pancrustacea hypothesis assumes a crusta- others 1989; Whitington and others 1993; Osorio and cean origin of insects or a sister group relationship others 1995; Whitington 1996; Dohle 1998; Nilsson between both groups (Zrzavy´ and Sˇtys 1997; Shultz and Osorio 1998; Duman-Scheel and Patel 1999; and Regier 2000; Dohle 2001; Mallatt and others Dohle 2001). Several independent phylogenetic ana- 2004; Regier and others 2005), and the Atelocerata lyses based on molecular data support a chelicerate/ hypothesis unites insects and myriapods as a clade myriapod sister group relationship, the so-called (Snodgrass 1938, 1950, 1951; Briggs and Fortey 1989; Myriochelata hypothesis (Friedrich and Tautz 1995; Schram and Emerson 1991; Bergstro¨m 1992; Wheeler Hwang and others 2001; Kusche and Burmester WC and others 1993; Kraus O and Kraus M 1994, 1996; 2001; Nardi and others 2003; Mallatt and others Emerson and Schram 1998; Wheeler WC 1998; Wills 2004; Pisani and others 2004), a link that had never and others 1998; Bitsch C and Bitsch J 2004). Whereas been considered by comparison of morphological the Atelocerata hypothesis is mainly supported by structures. However, recent comparative studies on morphological evidence, the idea of Pancrustacea neurogenesis in the diplopod Glomeris marginata was initially based on the phylogenetic analysis of and the chilopod Lithobius forficatus have shown that ribosomal-RNA sequence data in which crustaceans the myriapods and the chelicerates share several fea- and insects grouped together to the exclusion of tures that cannot be found in homologous form in 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. 1 E-mail: [email protected] 2 Present address: Johannes-Gutenberg University Mainz, Department of Genetics, Johann-Joachim-Becherweg 32, 55099 Mainz, Germany. Integrative and Comparative Biology, volume 46, number 2, pp. 195–206 doi:10.1093/icb/icj020 Advance Access publication February 16, 2006 Ó The Society for Integrative and Comparative Biology 2006. All rights reserved. For permissions, please email: journals.permissions@ oxfordjournals.org. 196 A. Stollewerk and A. D. Chipman 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; insects 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 crustaceans 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 chelicerates/myriapods the neighboring cells, which eventually leads to the activation of the E(spl) genes. The gene products of Fig. 1 Differences in the formation of neural precursors in this complex repress proneural gene expression, the arthropod groups. In insects and crustaceans, single which in turn leads to a down-regulation of Delta in neural precursors (neuroblasts) are specified. Whereas insect neuroblasts delaminate into the embryo shortly neighboring cells (Nakao and Campos-Ortega 1996; after formation, crustacean neuroblasts remain in the Ligoxygakis and others 1998). As a result of this feed- outer cell layer (neuroectoderm) and divide to give rise back loop, proneural gene expression is maintained in to ganglion mother cells that are pushed into the the neuroblast but down-regulated in the remaining interior of the embryo by directed mitosis. In both cells of the proneural cluster. Although this model chelicerates and myriapods, groups of neural precursors are selected and form invagination sites that eventually predicts a higher expression of Delta in single cells detach from the apical surface and differentiate into (presumptive neuroblasts), it has not been demon- neural cells. strated that Delta transcripts accumulate at higher levels in individual cells within the proneural clusters. Once a neuroblast is determined, it delaminates into insects and crustaceans. The most distinctive difference the embryo and divides asymmetrically to produce is that groups of neural precursors are singled out from ganglion mother cells (Goodman and Doe 1993). The the neuroectoderm of the spider and the myriapods, ganglion mother cells divide only once to give rise to rather than individual cells (that is, neuroblasts) as in neural cells that differentiate into neurons and glia. insects or crustaceans (Fig. 1) (Cupiennius salei: The neuroblasts do not delaminate all at once but Stollewerk and others 2001; Limulus polyphemus: in 5 discrete waves. Each neuroblast has a distinct iden- Mittmann 2002; C. salei: Stollewerk 2002; Stollewerk tity and gives rise to an invariant lineage of neural and others 2003; G. marginata: Dove and Stollewerk progenies. The identity of the neuroblasts is specified 2003; L. forficatus: Kadner and Stollewerk 2004). in the ventral neuroectoderm by segment polarity and Here we give an overview of the modes of neuro- dorsoventral patterning genes (see review in Skeath genesis in the major arthropod groups with special 1999). focus on myriapods and chelicerates. Furthermore, Neurogenesis has also been studied in insects we present new data on the geophilomorph centipede other than Drosophila. The pattern of neuroblasts is Strigamia maritima (Myriapoda) and discuss the data similar in all insects analyzed: they are arranged in in a phylogenetic context. 7 anteroposterior rows with 3–6 neuroblasts each (Bate 1976; Broadus and Doe 1995; Wheeler SR Neural precursor formation and others 2003). It has been shown in Tribolium in insects castaneum and in Schistocerca americana that single Neurogenesis has been studied in detail in the insect neuroblasts are selected in sequential waves, similar Drosophila melanogaster. The ventral neuroectoderm to D. melanogaster (Broadus and Doe 1995; Wheeler of the Drosophila embryo gives rise to both neural SR and others 2003). Within the insect group, and ectodermal cells (Jime´nez and Campos-Ortega proneural genes have been identified in several 1979, 1990; Cabrera and others 1987). The competence Diptera, a butterfly, and the flour beetle T. castaneum to adopt the neural fate depends on the presence of (Precis coenia: Galant and others 1998; Ceratitis the proneural genes achaete, scute, and lethal of scute. capitata:Wu¨lbeck and Simpson 2000; Calliphora These genes are expressed in clusters of cells in each vicina: Pistillo and others 2002; Phormia terranovae: Neurogenesis in myriapods and chelicerates
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