Establishment of the dorsoventral axis in nemertean embryos: Evolutionary considerations of spiralian development

The Nemertea represent one of a number of invertebrate phyla that display a highly conserved pattern of cell division known as spiral cleavage. The fates of the early blastomeres are known for representatives of some spiralian phyla (i.e., molluscs and annelids) and in these species there appears to be a high degree of conservation in the ultimate fates of particular embryonic cells. The first two cleavage planes bear an invariant relationship to the symmetry properties of the future larval and adult body plan. To investigate whether these properties of spiralian embryo-genesis are shared (conserved) amongst members of other spiralian phyla, individual blastomeres in two- and four-cell embryos of the nemertean, Nemertopsis bivittata, were microinjected with bi-otinylated dextran lineage tracers. N. bivittata is a direct-developing hoplonemertean that forms a nonfeeding larva. When individual blastomeres are injected at the two-cell stage, two sets of complementary labeling patterns (a total of four different patterns) were observed in the ectoderm of the larvae. When cells were injected at the four-cell stage, four different patterns were observed that represented subsets of the four patterns observed in the previous experiment. Unlike the case in the annelids and molluscs, in which the first cleavage plane bears a strict 45° angular relationship to the future dorsoventral axis, the first cleavage plane in N. bivittata can bear one of two different relationships relative to the larval/adult dorsoventral axis. In half the cases examined, the first cleavage plane corresponded roughly to the plane of bilateral symmetry, and in the rest, it lay along a frontal plane. A similar result was observed for the embryos of the indirect-developing heteronemertean, Cerebratutus lacteus. These results indicate that the fates of the four cell quadrants in nemerteans are not directly homologous to those in other spira-lians, such as the annelids and molluscs. For instance, no single cell quadrant appears to contribute a greater share to the formation of ectoderm, as is the case in the formation of the post-trochal region by the D-cell quadrant in annelids and mol-luscs. Rather, two adjacent cell quadrants contribute nearly equally to the formation of dorsal or ventral ectoderm in the larvae. Possible explanations for the determination of dorsoventrality in nemerte-ans, as well as implications of these findings regarding the evolution of spiralian development, are discussed. © 1994 Wiley-Liss, Inc.     

Cleavage in<Emphasis Type="Italic"> Nemertoderma westbladi</Emphasis> (Nemertodermatida) and its phylogenetic significance

Recent phylogenetic analyses of ribosomal and protein coding nuclear genes place the marine worms within the Nemertodermatida as one of the oldest lineages among the bilaterian animals. We studied the early embryonic cleavage in Nemertoderma westbladi to provide the first account of nemertodermatid early development. Live embryos were studied with interference microscopy and fixed embryos were either sectioned or studied with confocal laser scanning microscopy. Initially the divisions in the embryo are radial, but then micromeres are shifted clockwise generating a spiral pattern. The four-cell stage is characterized by duets of macromeres and micromeres and thus resembles the duet cleavage reported from members of the Acoela. However, subsequent stages differ from the acoel duet pattern and also from quartet spiral cleavage. The optimization of the cleavage pattern on current phylogenetic hypotheses with Nemertodermatida and Acoela as early bilaterian branches is discussed.     

The phylogenetic position of Brachiopoda—a comparison of morphological and molecular data

Analyses of rRNA and rDNA among Metazoa result in a hypothesis of a sistergroup relationship of Brachiopoda and certain spiralian taxa, whereas analyses of morphological data imply that Brachiopoda show affinities to Deuterostomia within the Radialia. Regarding Brachiopoda as a derived spiralian taxon must be followed by a reinterpretation of the evolution of distinct brachiopod morphological characters—like cleavage pattern, coelom or larva. The experimental insertion of a monophyletic taxon consisting of Brachiopoda and Phoronida into a widely accepted phylogenetic tree of Spiralia leads to the hypothesis that at least trimeric organization, mesosomal tentacular apparatus and heterogeneously assembled metanephridia are products of convergent evolution in Brachiopoda plus Phoronida and Deuterostomia. The hypothesis of a radialian nature of Brachiopoda and Phoronida, as implied by morphological data, remains as the most parsimonious possibility to explain the evolution of seven regarded characters (cleavage pattern, larva, tentacular apparatus, coelom, metameric segmentation, metanephridia and chaetae) in Brachiopoda. Due to the conflicting results of both methods a hitherto undetected systematical problem is discussed possibly hindering data comparability. If the course of evolution can principally be inferred from the information preserved in recent and fossil animals, the results should be congruent in the analyses of both, molecular and morphological data.     

R-spondins are involved in the ovarian differentiation in a teleost,medaka (Oryzias latipes)

Background

Among the four major bilaterian clades, Deuterostomia, Acoelomorpha, Ecdysozoa, and Lophotrochozoa, the latter shows an astonishing diversity of bodyplans. While the largest lophotrochozoan assemblage, the Spiralia, which at least comprises Annelida, Mollusca, Entoprocta, Platyhelminthes, and Nemertea, show a spiral cleavage pattern, Ectoprocta, Brachiopoda and Phoronida (the Lophophorata) cleave radially. Despite a vast amount of recent molecular phylogenetic analyses, the interrelationships of lophotrochozoan phyla remain largely unresolved. Thereby, Entoprocta play a key role, because they have frequently been assigned to the Ectoprocta, despite their differently cleaving embryos. However, developmental data on entoprocts employing modern methods are virtually non-existent and the data available rely exclusively on sketch drawings, thus calling for thorough re-investigation.

Results

By applying fluorescence staining in combination with confocal microscopy and 3D-imaging techniques, we analyzed early embryonic development of a basal loxosomatid entoproct. We found that cleavage is asynchronous, equal, and spiral. An apical rosette, typical for most spiralian embryos, is formed. We also identified two cross-like cellular arrangements that bear similarities to both, a "molluscan-like" as well as an "annelid-like" cross, respectively.

Conclusions

A broad comparison of cleavage types and apical cross patterns across Lophotrochozoa shows high plasticity of these character sets and we therefore argue that these developmental traits should be treated and interpreted carefully when used for phylogenetic inferences.     

Evolutionary Modifications of the Spiralian Developmental Program

SYNOPSIS. The Spiralia, an assemblage of phyla united by theirstereotypic pattern of early embryonic cell divisions (spiralcleavage), is an interesting group in which to investigate theevolution of development. This paper examines modificationsof developmental mechanisms within the Spiralia with emphasison the basallybranching forms. Although demonstrating a notabledegree of evolutionary conservation, the equal quartet cleavagepattern, which appears to be the ancestral condition, nonethelessexhibits modifications within the various spiralian groups,such as unequal cleavage, changes in cell size and rate of division,formation of two rather than four quadrants (duet spiral cleavage),and in extreme cases the loss of any trace of the spiral pattern.While the cell lineages of spiralians are remarkably conserved,one can discern evolutionary changes, for example in the cellsthat give rise to mesodenn. Studies of blastomere specificationin many spiralian groups and analyses of axis determinationindicate that embryos with equal versus unequal cleavage typicallyuse different determinative mechanisms to establish cell fatesand the dorsoventral axis. These properties are establishedearly in species exhibiting unequal cleavage. While previousexperiments suggested that equal cleavage was associated withlate specification, there is now evidence of precocious specificationof quadrant fates in some equal-cleaving species, such as thenemerteans and the polyclad turbellarians     

What studies of turbellarian embryos can tell us about the evolution of development mechanisms

In spiralian embryos determination of the axes of bilateral symmetry is associated with D quadrant specification. This can occur late through equal cleavage and cell interactions (conditional specification) or by the four-cell stage through unequal cleavage and cytoplasmic localization (autonomous specification). Freeman & Lundelius (1992) suggest that in spiralian coelomates the former method is ancestral and the latter derived, with evolutionary pressure to shorten metamorphosis resulting in early D quadrant determination through unequal cleavage and appearance of adult features in the larvae. Because of the key phylogenetic position of the turbellarian platyhelminthes, understanding the method of axis specification in this group is important in evaluating the hypothesis. Polyclad development, with equal quartet spiral cleavage, is believed to represent the most primitive condition among living turbellarians and has been examined experimentally in Hoploplana inquilina. Blastomere deletions at the two and four-cell stage produce larvae that are abnormal in morphology and symmetry, indicating that early development is not regulative, and also establish that the embryo does not have an invariant cell lineage. Deletions of micromeres and macromeres at the eight-cell stage indicate that cell interactions are involved in dorso-ventral axis determination, with cross-furrow macromeres playing a more significant role than non-cross-furrow cells. The results support the idea that conditional specification is the primitive developmental mode that characterized the common ancestor of the turbellarians and spiralian coelomates. Evolutionary trends in development in polyclads and other turbellarian orders are discussed.     

Changes in the pattern of cell arrangement at the surface of the shoot apical meristem in Hedera helix L. following gibberellin treatment

The changes in the pattern of cell arrangement and surface topography at the shoot apical meristem of Hedera helix L., which occur during gibberellic acid (GA₃)-induced transition from spiral to distichous phyllotaxis, were examined by scanning electron microscopy of rapidly frozen tissue. The technique preserves the original shape of the cells in their turgid state. It reveals distinct sets of radially oriented cell files, about four to eight cells wide, which extend from the central region of the meristem toward leaf primordia on the meristem flanks. In apices with spiral phyllotaxis, a new emerging primordium (0) appears as an acropetal bulge between the radial files adjacent to the third (3) and the second (2) older primordia. The bulging is associated with radial or oblique cell divisions while those located at the meristem flanks and in the radial files are oriented tangentially. As the displacement of existing primordia away from the central region increases following the GA₃ treatment, radial and oblique divisions as well as acropetal bulging invade the radial files adjacent to the primordium 2; consequently the angular divergence of the emerging primordium from the youngest existing primordium (1) increases. In apices with distichous phyllotaxis, the earliest bulging appears on both sides of the radial files facing primordium 2, with a slight depression at the files. The radial files therefore correspond to regions of the meristem where acropetal bulging is generally delayed, although this effect apparently diminishes with increasing distance of existing primordia from the meristem center.Abbreviations GA₃ gibberellic acid We thank Mr. Gilbert Ahlstrand, University of Minnesota, for his advice and assistance with the scanning electron microscopy. Contribution of the University of Minnesota Agricultural Experimental Station No. 19032.     

Cell Lineage of the Ilyanassa Embryo: Evolutionary Acceleration of Regional Differentiation during Early Development

Cell lineage studies in mollusk embryos have documented numerous variations on the lophotrochozoan theme of spiral cleavage. In the experimentally tractable embryo of the mud snail Ilyanassa, cell lineage has previously been described only up to the 29-cell stage. Here I provide a chronology of cell divisions in Ilyanassa to the stage of 84 cells (about 16 hours after first cleavage at 23°C), and show spatial arrangements of identified nuclei at stages ranging from 27 to 84 cells. During this period the spiral cleavage pattern gives way to a bilaterally symmetric, dorsoventrally polarized pattern of mitotic timing and geometry. At the same time, the mesentoblast cell 4d rapidly proliferates to form twelve cells lying deep to the dorsal ectoderm. The onset of epiboly coincides with a period of mitotic quiescence throughout the ectoderm. As in other gastropod embryos, cell cycle lengths vary widely and predictably according to cell identity, and many of the longest cell cycles occur in small daughters of highly asymmetric divisions. While Ilyanassa shares many features of embryonic cell lineage with two other caenogastropod genera, Crepidula and Bithynia, it is distinguished by a general tendency toward earlier and more pronounced diversification of cell division pattern along axes of later differential growth.     

Multiple,alternative cleavage patterns precede uniform larval morphology during normal development of Dreissena polymorpha (Mollusca,Lamellibranchia)

In this study we reinvestigate the early development of the freshwater mussel Dreissena polymorpha, previously studied by Meisenheimer (1901). The data include video time-lapse recordings of living embryos and bisbenzimide stains of fixed embryos as well as morphometry on fixed, serially-sectioned embryos. We present the cell lineage and cell cycle durations up to the first indication of symmetrization within this embryo. We show that early cell cycles last approximately 1h. A dramatic extension of cell cycle duration and a concomitant asynchrony among the various cell lines was observed starting at the fifth cleavage. Short cell cycles, like those of early blastomeres, were a constant property of the largest descendants of the 2d-cell line only. In contrast to Meisenheimer's observations and our experiences with other spiralian embryos, the cleavage pattern proved to follow multiple alternatives. The embryonic quadrants A-D were arranged in either a clockwise or counter-clockwise fashion and the chirality of the third cleavage was either dextral or sinistral irrespective of the arrangement of the quadrants. As a consequence, four different blastomere configurations were encountered and the dorsoventral axis could take four different angles with respect to the plane of first cleavage. The dorsal side was most easily recognized by the position of the 2d-micromere at the 16-cell stage. The fact that all of such embryos could develop into normal, uniform larvae is interpreted as the result of cell-cell interactions in morphogenetic regulation.     

Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae

A growing body of data from nervous systems of marine invertebrate larvae provides an ideal background for comparisons among higher taxa. The currently available data from Bryozoa, however, do not allow for a consistent hypothesis of an ancestral state for this taxon, which would be necessary for phylogenetic inferences. The larval nervous systems of the four gymnolaemate species Flustrellidra hispida, Bugula fulva, Alcyonidium gelatinosum, and Bowerbankia gracilis are examined by means of antibody staining against the neurotransmitters serotonin and FMRFamide, as well as against acetylated α-tubulin. Despite considerable variation, a comparison reveals a common pattern of the distribution of serotonin. The neurotransmitter is found in at least two cells in the apical organ as well as in paired axial and lateral nerves emerging from a central nerve nodule. A ring nerve is present below the corona and at least two serotonergic cells are found between the corona cells. Serotonergic coronal cells might represent unique bryozoan features, whereas the remaining elements show resemblance to the situation found in most spiralian taxa. The data do not provide support for a closer relationship of Bryozoa to Phoronida or Brachiopoda.     

Spiralian quartet developmental potential is regulated by specific localization elements that mediate asymmetric RNA segregation

Spiralian embryos are found in a large group of invertebrate phyla but are largely uncharacterized at a molecular level. These embryos are thought to be particularly reliant on autonomous cues for patterning, and thus represent potentially useful models for understanding asymmetric cell division. The series of asymmetric divisions that produce the micromere quartets are particularly important for patterning because they subdivide the animal-vegetal axis into tiers of cells with different developmental potentials. In the embryo of the snail Ilyanassa, the IoLR5 RNA is specifically segregated to the first quartet cells during the third cleavage. Here, we show that this RNA, and later the protein, are maintained in the 1q(121) cells and their descendents throughout development. Some IoLR5-expressing cells become internalized and join the developing cerebral ganglia. Knockdown of IoLR5 protein results in loss of the larval eyes, which normally develop in association with these ganglia. Segregation of this RNA to the first quartet cells does not occur if centrosomal localization is bypassed. We show that the specific inheritance of the RNA by the first quartet cells is driven by a discrete RNA sequence in the 3' UTR that is necessary and sufficient for localization and segregation, and that localization of another RNA to the first quartet is mediated by a similar element. These results demonstrate that micromere quartet identity, a hallmark of the ancient spiralian developmental program, is controlled in part by specific RNA localization motifs.     

Some aspects of spiralian development

Nielsen, C. 2010. Some aspects of spiralian development. —Acta Zoologica (Stockholm) 91 : 20–28 Spiralian development is not only a characteristic early cleavage pattern, with shifting orientations of the cleavage planes, but also highly conserved cell lineages, where the origin of several organs can be traced back to identifiable cells in the lineage. These patterns are well documented in annelids, molluscs, nemertines, and platyhelminths and are considered ancestral of a bilaterian clade including these phyla. Spiral cleavage has not been documented in ecdysozoans, and no trace of the spiral development pattern is seen in phoronids and brachiopods. Origin of the spatial organization in spiralian embryos is puzzling, but much of the information appears to be encoded in the developing oocyte. Fertilization and “pseudofertilization” apparently provides the information defining the secondary, anterior‐posterior body axis in many species. The central nervous system consists of three components: an apical organ, derived from the apical blastomeres 1a¹¹¹‐1d¹¹¹, which degenerates before or at metamorphosis; the cerebral ganglia derived from other blastomeres of the first micromere quartet and retained in the adult as a preoral part of the brain; and the originally circumblastoporal nerve cord, which has become differentiated into a perioral part of the brain, the paired or secondarily fused ventral nerve cords, and a small perianal nerve ring.     

Cell lineage and fate map of the primary somatoblast of the polychaete annelid Capitella teleta

Like most polychaete annelids, Capitella teleta (formerly Capitella sp. I) exhibits a highly stereotypic program of early development known as spiral cleavage. Animals with spiral cleavage have diverse body plans, and homologous embryonic cells can be readily identified among distantly related animals. Spiralian embryos are particularly amenable to studies of fate-mapping, and larval fates of identified cells are conserved among diverse taxa. One cell of particular importance in spiralian development is 2d, or the primary somatoblast, which generates ectoderm of the body posterior to the prototroch. We are interested in the evolution of the primary somatoblast, and thus far, the 2d sublineage has only been analyzed in a few species. In Capitella teleta, 2d generates ectoderm of the segmented trunk and post-segmental pygidium. In this study, development of the 2d lineage was characterized in detail through intracellular injections of DiI, and time-lapse as well as confocal microscopy to analyze cleavage patterns and the fates of larval cells. Analysis of cleavage patterns reveals that the first bilateral division in the 2d sublineage occurs with the division of 2d112, the same 2d daughter cell that first divides bilaterally in the polychaete Platynereis dumerilii. Larval fates of blastomeres 2d1, 2d2, 2d11, 2d12, 2d112, 2d1121, and 2d1122 were determined. All cells show stereotypic descendant clones that are consistent with segregation within sublineages. In the first few divisions of the 2d sublineage, larval-specific structures (neurotroch and telotroch) and pygidial ectoderm are segregated from segmental ectoderm and ventral nerve cord. The daughters of the first bilateral division, 2d1121 and 2d1122, generate the right and left halves of the segmental ectoderm and ventral nerve cord respectively, although the clones are consistently asymmetric across the dorsal midline. The pattern of cleavage divisions and the fates of the 2d daughters in Capitella teleta are compared to those in other spiralians with special attention to annelids.     

Widespread RNA segregation in a spiralian embryo

Asymmetric cell divisions are a crucial mode of cell fate specification in multicellular organisms, but their relative contribution to early embryonic patterning varies among taxa. In the embryo of the mollusc Ilyanassa, most of the early cell divisions are overtly asymmetric. During Ilyanassa early cleavage, mRNAs for several conserved developmental patterning genes localize to interphase centrosomes, and then during division they move to a portion of the cortex that will be inherited by one daughter cell. Here we report an unbiased survey of RNA localization in the Ilyanassa embryo, and examine the overall patterns of centrosomal localization during early development. We find that 3-4% of RNAs are specifically localized to centrosomes during early development, and the remainder are either ubiquitously distributed throughout the cytoplasm or weakly enriched on centrosomes compared with levels in the cytoplasm. We observe centrosomal localization of RNAs in all cells from zygote through the fifth cleavage cycle, and asymmetric RNA segregation in all divisions after the four-cell stage. Remarkably, each specifically localized message is found on centrosomes in a unique subset of cells during early cleavages, and most are found in unique sets of cells at the 24-cell stage. Several specifically localized RNAs are homologous to developmental regulatory proteins in other embryos. These results demonstrate that the mechanisms of localization and segregation are extraordinarily intricate in this system, and suggest that these events are involved in cell fate specification across all lineages in the early Ilyanassa embryo. We propose that greater reliance on segregation of determinants in early cleavage increases constraint on cleavage patterns in molluscs and other spiralian groups.     

Pattern Formation in the Arabidopsis Embryo Revealed by Position-Specific Lipid Transfer Protein Gene Expression

During Arabidopsis embryogenesis, the zygote divides asymmetrically in the future apical-basal axis; however, a radial axis is initiated only within the eight-celled embryo. Mutations in the GNOM, KNOLLE, and KEULE genes affect these processes: gnom zygotes tend to divide symmetrically; knolle embryos lack oriented cell divisions that initiate protoderm formation; and in keule embryos, an outer cell layer is present that consists of abnormally enlarged cells from early development. Pattern formation along the two axes is reflected by the position-specific expression of the Arabidopsis lipid transfer protein (AtLTP1) gene. In wild-type embryos, the AtLTP1 gene is expressed in the protoderm and initially in all protodermal cells; later, AtLTP1 expression is confined to the cotyledons and the upper end of the hypocotyl. Analysis of AtLTP1 expression in gnom, knolle, and keule embryos showed that gnom embryos also can have no or reversed apical-basal polarity, whereas radial polarity is unaffected. knolle embryos initially lack but eventually form a radial pattern, and keule embryos are affected in protoderm cell morphology rather than in the establishment of the radial pattern.     

Quantitative analysis of cellular differentiation during early embryogenesis ofPlatynereis dumerilii

Summary As in many spiralian embryos with unequal cleavage, cleavage inPlatynereis follows an invariant pattern. Preceding each cleavage the cytoplasm is reorganized, allowing the spiral cleavage mode to produce cells with different cytoplasmic composition. The fertilized egg undergoes a dramatic ooplasmic segregation after the completion of the cortical reaction. As a consequence, a plug of clear cytoplasm becomes located at the animal pole. Once the four quadrants of the embryo have been established, the cleavage sequence of the D quadrant differs clearly from that of the other three quadrants. The results presented here suggest that differential distribution of the clear cytoplasm governs this sequence. The first quartet of micromeres, which will form the ectoderm and the cerebral ganglia of the head, is clearly bilaterally symmetrical from the onset of the third cleavage. Dorsoventral polarity and bilateral symmetry in the ectoderm of the trunk is expressed most markedly by the dorsal location of the large 2d cell, whose rapid proliferation is bilaterally symmetrical with respect to the median plane. As a result of this proliferation it comes to fill most of the posttrochal region (ectoderm, three pairs of anlagen for the setal sacs, and the ventral plate which forms the nerve cord). The other micromeres contribute only a minor portion of the ventral ectoderm and are involved in the formation of the stomodaeum. The mesentoblast, 4d, i.e. the stem cell of the primary mesoderm, forms at the sixth cleavage, also in a position on the dorsal mid-line. The daughter cells, which arise from 4d by strictly bilaterally symmetrical cleavage, form the mesodermal germ bands, which lie beneath the ectoderm. The trochoblasts are formed by asynchronously cleaving founder cells, but further cleavages in these cells are synchronous. This suggests that cell-cell interaction is involved in the development of this alleged mosaic embryo.     

A Stereometric Analysis of Karyokinesis, Cytokinesis and Cell Arrangements during and following Fourth Cleavage Period in the Sea Urchin, Lytechinus variegatus

Fourth cleavage of the sea urchin embryo produces 16 blastomeres that are the starting point for analyses of cell lineages and bilateral symmetry. We used optical sectioning, scanning electron microscopy and analytical 3-D reconstructions to obtain stereo images of patterns of karyokinesis and cell arrangements between 4th and 6th cleavage. At 4th cleavage, 8 mesomeres result from a variant, oblique cleavage of the animal quartet with the mesomeres arranged in a staggered, offset pattern and not a planar ring. This oblique, non-radial cleavage pattern and polygonal packing of cells persists in the animal hemisphere throughout the cleavage period. Contrarily, at 4th cleavage, the 4 vegetal quartet nuclei migrate toward the vegetal pole during interphase; mitosis and cytokinesis are latitudinal and subequatorial. The 4 macromeres and 4 micromeres form before the animal quartet divides to produce a 12-cell stage. Subsequently, macromeres and their derivatives divide synchronously and radially through 8th cleavage according to the Sachs-Hertwig rule. At 5th cleavage, mesomeres and macromeres divide first; then the micromeres divide latitudinally and unequally to form the small and large micromeres. This temporal sequence produces 28-and 32-cell stages. At 6th cleavage, macromere and mesomere descendants divide synchronously before the 4 large micromeres divide parasynchronously to produce 56- and 60-cell stages.     

Myosin and actin are necessary for polar lobe formation and resorption in Ilyanassa obsoleta embryos

 During the first mitotic divisions many spiralian embryos form a cytoplasmic protrusion at the vegetal pole called the polar lobe. In the gastropod Ilyanassa obsoleta the polar lobe is constricted by a contractile ring composed of filamentous actin, myosin, and associated proteins, similar to the contractile ring of the cleavage furrow. To resolve the role of myosin and actin in polar lobe formation and resorption, we have applied 2,3-butanedione monoxime and Latrunculin B at different stages of the first cleavage to inhibit myosin and F-actin, respectively. Our results show that myosin is important for both cytokinesis and polar lobe formation. Additionally, we have found that the resorption of the polar lobe is a two-step process: the first step is passive, driven by the tension of the actin-cortex and the second step is active, in which the ATP-hydrolysis of myosin/actin interaction supplies the force to complete the resorption of the polar lobe. We have summarized our results in a scheme of the first cleavage of Ilyanassa obsoleta. Received: 6 November 1997 / Accepted:15 March 1998     

Cleavage and gastrulation in the shrimp Penaeus (Litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata)

While most malacostracan crustaceans develop through superficial cleavage, in the Amphipoda, Euphausiacea, and Dendrobranchiata (Decapoda) cleavage is complete. Euphausiaceans and dendrobranchiate shrimp share a similar early cleavage pattern, early cleavage arrest and ingression of mesendoderm progenitor cells, a ring of crown cells (prospective naupliar mesoderm) around the blastopore, and hatching as a nauplius larva. Yet recent phylogenies do not support a close relationship between Euphausiacea and Decapoda. In addition, some variation is reported in the timing of mesendoderm cell arrest and number of crown cells for a number of dendrobranchiates. To determine the representative pattern of development in the Dendrobranchiata, embryos of the Pacific white shrimp Penaeus (Litopenaeus) vannamei were stained with Sytox Green to label chromosomes and nuclei and examined with confocal microscopy. The early cleavage pattern, mesendoblast arrest and subsequent ingression at the 32-cell stage, presence of 8 initial crown cells, and fates of the mesendoblasts are the same for P. vannamei (family Peneaeidae) and Sicyonia ingentis (family Sicyoniidae). The lineage of the primordial endoderm cells differs from that reported for P. kerathurus. These characters were discussed in the context of the evolution of development in the Dendrobranchiata and in comparison to the Euphausiacea.