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The Spider Parasteatoda Tepidariorum

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The Spider Parasteatoda Tepidariorum PRIMER SERIES PRIMER 2655 Development 139, 2655-2662 (2012) doi:10.1242/dev.078204 © 2012. Published by The Company of Biologists Ltd Evolutionary crossroads in developmental biology: the spider Parasteatoda tepidariorum Maarten Hilbrant1, Wim G. M. Damen2 and Alistair P. McGregor1,* Summary Stollewerk et al., 2003; Telford and Thomas, 1998) and are likely Spiders belong to the chelicerates, which is an arthropod group to continue to do so. However, Parasteatoda is now the most that branches basally from myriapods, crustaceans and insects. commonly used chelicerate model for developmental studies, Spiders are thus useful models with which to investigate particularly with respect to embryogenesis (McGregor et al., 2008a; whether aspects of development are ancestral or derived with Oda and Akiyama-Oda, 2008). This is in part owing to the platform respect to the arthropod common ancestor. Moreover, they serve provided by classical embryological studies of spider development as an important reference point for comparison with the (reviewed in Anderson, 1973), the ease of culturing Parasteatoda, development of other metazoans. Therefore, studies of spider its short life cycle, year-round access to all embryonic stages, and development have made a major contribution to advancing our an expanding range of genetic resources and functional tools understanding of the evolution of development. Much of this (McGregor et al., 2008a). knowledge has come from studies of the common house spider, We reasoned previously that further studies of the spiders Parasteatoda tepidariorum. Here, we describe how the growing Parasteatoda and Cupiennius could provide new insights into number of experimental tools and resources available to study developmental mechanisms and their evolution (McGregor et al., Parasteatoda development have provided novel insights into the 2008a). In this Primer, we now review the advances made in these evolution of developmental regulation and have furthered our areas using Parasteatoda as a model. Specifically, we describe the understanding of metazoan body plan evolution. development of Parasteatoda and summarise the range of tools and resources available that have facilitated the identification of several Key words: Axis formation, Evolution, Gene regulation, fundamental aspects of developmental regulation. We also Segmentation, Spiders highlight the potential for gaining further insights into the evolution of developmental mechanisms by the continuing development of Introduction this model, which is used by a growing community of researchers. The common house spider Parasteatoda tepidariorum (formerly known as Achaearanea tepidariorum) (Saaristo, 2006) is an Life cycle and development excellent model organism with which to investigate developmental Female Parasteatoda lay clutches of up to 400 eggs (Miyashita, mechanisms and their evolution. Spiders belong to the chelicerates 1987; McGregor et al., 2008a) of ~0.5 mm in diameter, and wrap (see Glossary, Box 1), which branch at the base of the arthropods these in a protective silk egg sack or cocoon (Montgomery, 1903). (Fig. 1), and therefore represent a sister group to the other extant Eggs are fertilised during oviposition (Montgomery, 1907), which arthropod phyla, myriapods, crustaceans and insects (see Glossary, takes ~3-4 minutes (Montgomery, 1903), resulting in the embryos Box 1) (Regier et al., 2010; Rota-Stabelli et al., 2010). Given the in each cocoon developing in concert. The first divisions of the phylogenetic position of Parasteatoda, comparing its development energids (see Glossary, Box 1) occur in the centre of the spherical with that of other arthropods and ecdysozoa (see Glossary, Box 1), centrolecithal eggs (see Glossary, Box 1). Although precisely when can be useful in helping to identify which aspects of development cellularisation takes place remains to be determined, it appears to are possibly ancestral or derived among these animals, and even occur before the fifth division cycle while the nuclei within the other metazoans. Studies of spiders have also been insightful for energids are migrating from the centre to the periphery of the yolk understanding general developmental concepts, ranging from cell mass (Kanayama et al., 2010). At the 64-cell stage, at ~11 hours migration to differentiation (e.g. Akiyama-Oda and Oda, 2010; after egg laying (hAEL) at 25°C, the cells are visible on the surface Stollewerk and Seyfarth, 2008), and they have proven to be of the embryo and the blastoderm forms (Kanayama et al., 2010; particularly good models for investigating the regulation of Montgomery, 1909) (Fig. 2A, stage 2). The cells continue to divide segmentation (Damen, 2007; Minelli and Fusco, 2004). Moreover, and gradually converge towards one pole of the egg. At 25-30 spider embryogenesis exhibits features, for example a structure hAEL, this leads to the formation of a cell-dense, dome-shaped called the cumulus (see Glossary, Box 1) (Oda and Akiyama-Oda, germ disc (see Glossary, Box 1) and a region that contains a few 2008), that are not known in other arthropod models, and studies of scattered, putatively extra-embryonic, cells (Akiyama-Oda and these animals can therefore also enrich our knowledge of the Oda, 2003; Montgomery, 1909) (Fig. 2A, stage 4). diversity of developmental mechanisms used among animals. Between 55 and 65 hAEL, gastrulation and a series of complex Studies of other chelicerates, including the Central American cell movements take place, and the onset of segmentation is wandering spider Cupiennius salei, have made a valuable observed (described in more detail below). This transforms the contribution to understanding developmental evolution (e.g. initial radially symmetrical germ disc into a multilayered short germ band (see Glossary, Box 1) with bilateral symmetry 1Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy (Akiyama-Oda and Oda, 2003; Kanayama et al., 2011) (Fig. 2A, Lane, Oxford OX3 0BP, UK. 2Department of Genetics, Friedrich Schiller University stage 8). Between 65 and ~90 hAEL, during a period of Jena, Philosophenweg 12, 07743 Jena, Germany. development comparable to Cupiennius stages 9 to 12 (Wolff and *Author for correspondence ([email protected]) Hilbrant, 2011), most segments of the opisthosoma (see Glossary, DEVELOPMENT 2656 PRIMER Development 139 (15) Chelicerata (Parasteatoda, Cupiennius) Box 1. Glossary Arthropoda Centrolecithal eggs. Eggs in which the yolk is concentrated in the Myriapoda (Strigamia, Glomeris) Mandibulata centre of the cytoplasm. Chelicerates. A group of arthropods that includes spiders, mites, Hexapoda (Drosophila, Tribolium) scorpions and harvestmen, and also horseshoe crabs, for which the oldest known fossil dates back to the Upper Ordovician (circa 445 Crustacea (Parhyale, Daphnia) Ma) (Redkin et al., 2008). Crustaceans. A group of arthropods that includes lobsters, crabs, Onychophora (Euperipatoides) shrimps and woodlice. Cumulus mesenchyme (CM) and cumulus. The CM is a group Nematoda (Caenorhabditis) of endodermal cells that migrates away from the primary thickening towards the periphery of the germ disc. CM cells closely associate Fig. 1. Phylogenetic relationships between arthropoda and with the germ disc epithelium on their trajectory, and this related phyla. For each of the phyla, the genera of two selected interaction induces DV axis formation. Together, CM and model organisms are shown in parentheses. The red circle indicates the epithelium form a clump that bulges out from the surface, branch point of the Chelicerata and the Mandibulata (Myriapoda, conventionally called the cumulus. Hexapoda, Crustacea). Outgroups to the Arthropoda, represented by Cytoneme. A long and thin plasma-membrane projection oriented velvet worm Euperipatoides and nematode Caenorhabditis genera, are towards a morphogen-producing cell (Ramírez-Weber and shown in grey (Regier et al., 2010; Rota-Stabelli et al., 2010). Kornberg, 1999). Dorsal field. The extra-embryonic tissue that appears after the cumulus has migrated through the germ disc. Ecdysozoa. The name given to all moulting animals (including arthropods and nematodes), based on an influential phylogenetic Embryonic development takes about eight days at 25°C. The study that used ribosomal RNA sequences (Aguinaldo et al., 1997) largely immotile postembryo (Downes, 1987) then ecloses but and resulted in new views on the phylogenetic relationships of remains within the protection of the cocoon (Fig. 2A, postembryo). animals (Adoutte et al., 2000). The first moult then takes place after about two days, and gives rise Energid. A nucleus and the cytoplasm with which it interacts during the early superficial cleavages. to the first instar (Fig. 2A), which leaves the cocoon. The period Germ disc. An aggregation of blastoderm cells forming the from leaving the cocoon to reaching adulthood takes a minimum embryonic primordium. Note that the word ‘disc’ is slightly of 30 days with four to six moults for males, and 40 days with five misleading as the primordium is dome shaped and not flat. to seven moults for females (Miyashita, 1987) (Fig. 2A). After the Insects. A group of hexapod arthropods that includes beetles, flies, females reach adulthood they become receptive to mating with grasshoppers and dragonflies. The body of insects is made up of a male spiders (Fig. 2B). In parallel, vitellogenesis begins and a head, thorax and abdomen. female can produce her first clutch of eggs as soon as one week Myriapods. A group of arthropods
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