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Contributions to Zoology, 71 (1/2) 9-28 (2002) Contributions to Zoology, 71 (1/2) 9-28 (2002) SPB Academic Publishing bv, The Hague and disc formation of the Orchestia Cleavage, gastrulation, germ amphipod cavimana (Crustacea, Malacostraca, Peracarida) Gerhard Scholtz & Carsten Wolff Institut 10115 Humboldt-Universität zu Berlin, für Biologie/Vergleichende Zoologie, Philippstr. 13, Berlin, Germany, e-mail: [email protected] Keywords: cell lineage, cell migration, Arthropoda, phylogeny, evolution Abstract Contents Investigations ofamphipod embryonic developmenthave a long Introduction 9 tradition. of Material and methods 10 However, many aspects amphipodembryology are still the of the animals controversial. These concern, among others, nature of Maintaining and embryos 10 the the of the the of Live observation 11 cleavage, origin germ disc, and mode gastrulation. On the other hand, amphipods show the same Video recording 11 characteristic the and type ofinvariant cell division pattern in germ Histology scanning electron microscopy 11 band as other malacostracans. Since amphipods seem to undergo Injections 11 a stereotyped pattern ofearly cleavage they are highly interesting Nomenclature 12 for our understanding ofthe evolution ofarthropod development. Results 12 In this The first four paper, we describe the cleavage patternof the amphipod cleavages 12 crustacean The and further Orchestia cavimana from the zygote to gastrulation fifth cleavage 14 and the formation of Mirror the germ disc using direct observation, images 17 The of scanning electron microscopy, histology, video recording, and formation the germ disc 17 lineage with follows Gastrulation tracing a vital dye. The early development 19 the mode of a total, radial, unequalcleavage with a determinate Discussion 22 stereotyped pattern. A small transient blastocoel is formed.The A secondary meroblastic radial cleavage despite 8-cell is stage characterisedby 4 micromeres and 4 macromeres. yolky eggs 22 One quadrant is smaller than the others. There are two kinds of Mirror images 24 e ggs that show The is the of the disc of a mirror handed image. 16-cell stage Origin germ by migrations macromere last regular stage after which the blastomeres divide highly derivatives 24 - The disc is formed the descendants Gastrulation in the asynchronously. germ by amphipods only “protostome” of the The other malacostracan macromeres and some micromere derivatives. crustaceans 25 micromeres constitute the extra-embryonic region. Migration The embryonic development ofamphipods shows of macromere descendants is involved in disc formation germ many apomorphic characters 25 accompanied by the extrusion ofthe yolk. During this process Acknowledgements 26 some vitellophages are formed. The gastrulation sensu stricto References 27 is initiated by the micromere derivatives ofthe smallest quadrant at the anterior ofthe disc. A forming germ true blastopore occurs which involves an invagination and the immigration of cells. Introduction Our data help to correct erroneousinterpretations of former students of We show that amphipod development. can many chaiacters of The of amphipod embryonic developmentare apomorphic early development arthropods exhibits a great supporting amphipodmonophyly. With the present investigation variety of modes with respect to virtually all as- we contribute to a complete understanding of the embryonic at level. We find all sorts cell pects every of cleavage lineage of from the formation amphipods egg to segment and modes from total to superficial (Anderson 1973; organogenesis. Scholtz 1997), different ways of gastrulation (Wey- goldt 1979), numerous modes of germ band for- Downloaded from Brill.com10/09/2021 12:09:51AM via free access 10 G. Scholtz & C. Wolff- Embryonic development in amphipods (Crustacea) and of 8-cell mation segmentation processes (Scholtz 1997), originates from the micromeres the stage. and all kind of larval direct In and stages up to develop- contrast, Langenbeck (1898) Rappaport ment (Anderson 1973). This diversity at the cellu- (1960) found that the macromeres of the 8-cell stage rise to the disc cells. lar, morphological and ecological levels is also give germ Furthermore, some authors that the reflected at the genetic level where early pathways suggested cleavage pattern of shows of are evolutionarily altered despite a similar result- amphipods aspects spiral cleavage (Sheader & Shia which has been denied other ing or subsequent pattern (Abzhanov & Kaufman 1970) by re- searchers 1997; Wolff & Scholtz 1999; Jockusch et al. 2000; Davis & Patel 2002). (Scholtz 2002). In order to a better of This high degree of variation can be found even gain picture early amphi- we several such within arthropod subgroups such as malacostracan pod development applied techniques as direct observation of embryos, video re- crustaceans or hymenopteran insects (Grbic 2000; living Scholtz 2000). cording, scanning electron microscopy (SEM), plas- tic for and the vital Dil The present study describes the early cell lin- embedding histology, dye to cell In and disc as a marker study lineage. particular, we eage during cleavage, gastrulation germ address the in- following questions: what of cleav- formation of an amphipod crustacean. Although type total radial? age occurs, or superficial, spiral or vestigations on amphipod embryology started as Where do the germ disc cells come from? When early as 1837 with Rathke’s report, there are still are the axes of the determined? What kind controversial views and con- embryo many open questions In of gastrulation is found? a first we traced cerning the exact mode of amphipod embryonic paper, the fate of individual cells of the 8- and 16-cell development. Like all other malacostracans studied, & Here describe stages (Wolff Scholtz 2002). we amphipods undergo a distinct stereotyped pattern the cleavage pattern in detail, the formation of the of cell divisions from the formation of the post- germ disc, and the gastrulation process. naupliargerm band up to segmentation, neurogenesis, Our results confirm that the amphipod Orchestia limb bud formation, and mesodermal differentiation shows total cleavage with a highly stereotyped cell (Dohle & Scholtz 1988; Scholtz & Dohle 1996; lineage. The germ disc is formed by derivatives of Scholtz et al. 1994; Scholtz 1990,2000; Gerbcrding both micromeres and macromeres with the mac- & Scholtz 1999, 2001). However, most of the de- romeres giving rise to the largest part of the ecto- capod and peracarid species studied with respect derm and to mesendodermal parts of the embryo in to their cell lineages the germ band undergo a whereas the micromeres contribute partly to the superficial cleavage that does not allow the tracing mesendodennand to the extra-embryonic ectoderm. of early cell lineages (if at all present) up to germ The cleavage is not spiral. Gastrulation takes place disc formation and gastrulation. This is different at the anterior end of the disc. germ in amphipods; there is some evidence from several The general pattern of early amphipod develop- studies that the early cleavage of amphipods shows ment is malacostracans and crusta- unique among a stereotyped pattern (e.g. van Beneden& Bessels ceans in general. It shows a numberof apomorphic 1869; Ulianin 1881; Langenbeck 1898; Heidecke characters related to cleavage, gastrulation, germ 1904; Rappaport 1960; Brcgazzi 1973; Meschen- band proliferation, and gene expression unifying moser 1987). However, in some respects these in- the different amphipod taxa. vestigations led to contradictory results. For instance, La Valettc St. George (I860), Ulianin (1881) and Mergault & Charniaux-Cotton (1973) claimed that Material and methods the cleavage is not total but that the central yolk mass remains undivided whereas authors such as Maintaining of the animals and embryos Langenbeck (1898) and Percyaslawzewa (1888a) suggested a clear total cleavage mode. Several Specimens of the terrestrial amphipod species Or- authors (e.g. Ulianin 1881; Bregazzi 1973; Mergault chestia cavimana were collected from beaches of & Charniaux-Cotton 1973) stated that the germ disc the Tegeler See (Berlin) and from the river Weser Downloaded from Brill.com10/09/2021 12:09:51AM via free access Contributions to Zoology, 71 (1/3) - 2002 11 close to the town ofElsfleth where they live in and Sony SSC-M370CE, analogous recorder: Panaso- feed detritus on (Rudolph 1995). The animals were The was one minute. nic). frequency picture per terrarium 18-20°C maintained in a at and fed with Later the recorded sequences were digitised. The carrots and rolled oats. To receive in relevant eggs video films are put on the homepage of Contribu- the animal in stages a so-called praecopula (the male tions to Zoology thttp://www.uba.uva.nl/ctz). carries the female around for a while before copu- lation) were caught and isolated. Usually after about 10-14 hours the animals and the female’s separate Histology and scanning electron microscopy ventral brood pouch (marsupium) contains eggs in an early stage of cleavage. Females with in For eggs semi-thin sections the embryos were fixed for their where dazed in mineral marsupium carefully 30 min to 2 h in buffered 5% formaldehyde, Bouin’s water C0 The were washed containing . eggs out solution or a mixture of acid and sublimate. 2 picric of the marsupium from anterior with a Pasteur The pi- egg envelopes were removed during fixation pette. The were transferred salt dishes eggs to con- (if possible) to allow better penetration. After wash- taining a saline which mimicks the in the in and liquid ing distilled water a dehydration in an etha- marsupium saline saline = series the (isopod : NaCI-frog 1:2; nol embryos were transferred to the meta- [ saline: isopod 12 g NaCl, 1,6 g KC1, 1,6 CaCl medium g , crylate embedding 2 (Technovit) following 1,6 g NaHC0 1 I MgCl,, 0,2 g to aqua desk; NaCI- standard Serial semi-thin sections 3 protocols. (3pm) frog saline: 115 mM 2,5 mM KC1, 2,15 NaCl,' mM were produced with a Jung microtome. Toluidine- Na,HP0 mM mM *2H,0, 0,85 NaH,P0 *H,0, 1,8 blue was used for Some whole-mount 4 4 staining. CaCl 7 *H,0]). done of of preparations were eggs various stages.
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