Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Lyons, Deirdre C.; Perry, Kimberly J.; Lesoway, Maryna P.; Henry, Jonathan J.

doi:10.1186/2041-9139-3-21

Cited by 68 publications

(96 citation statements)

References 90 publications

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“…7 A,A'). Autofluorescence of the absorptive cells has also been reported in C. fornicata (Lyons et al, 2012). Post-gastrula-like embryos also show ciliated outgrowths of cells, thickened epidermal cells, and infrequently grow eyespots (Fig.…”

Section: Development Of Nutritive Embryos: Post-gastrula-like Embryosmentioning

confidence: 80%

The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella

Lesoway

Abouheif²,

Collin³

2014

Int. J. Dev. Biol.

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Adelphophagy occurs when encapsulated embryos complete development by feeding on their developing siblings, which are known as nutritive embryos. Nutritive embryos are found in a variety of animal groups, and are especially common in some groups of marine invertebrates. Although they have evolved numerous times independently in the calyptraeid gastropods, adelphophagic development with nutritive embryos has not been described in detail. Using light microscopy and time-lapse imaging of laboratory-reared embryos, we describe the development of Crepidula navicella, a direct developer with nutritive embryos that cleave and gastrulate. Early stages of nutritive and viable embryos do not show any obvious morphological differences, but do show asynchrony in early cleavage among embryos from the same capsule. We discovered that two classes of nutritive embryos are produced; gastrula-like nutritive embryos, which arrest after gastrulation, and post-gastrula-like nutritive embryos that are more variable in morphology, and show evidence of minor differentiation. This study provides a framework for future research on the developmental and molecular mechanisms of nutritive embryo development of C. navicella, which will allow us to address the role of nutritive embryos in the origins of developmental polyphenisms. Careful description of the developmental sequence is necessary before adaptive hypotheses can be addressed, and comparisons with other taxa can be made. Understanding the different ways that embryos and their development are disrupted to produce nutritive embryos will provide important insights into the normal process of development.

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Section: Development Of Nutritive Embryos: Post-gastrula-like Embryosmentioning

confidence: 80%

The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella

Lesoway

Abouheif²,

Collin³

2014

Int. J. Dev. Biol.

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“…Additional work was carried out by their counterparts in Europe (e.g., Heymons, 1893;Wierzejski, 1905). That early work has been extended in recent decades using modern cell-autonomous lineage tracers for a number of species (i.e., the gastropod molluscs Crepidula fornicata and C. convexa, Hejnol et al, 2007;Lyons et al, 2012, and Ilyanassa obsoleta, Render 1991, 1997Chan and Lambert 2014; the polyplacophoran mollusc, Chaetopleura apiculata, Henry et al, 2004; the nemerteans, Cerebratulus lacteus, Carinoma tremaphoros, Maslakova et al, 2004a,b; the polyclad turbellarian Hoploplana inquilina, Boyer et al, 1996Boyer et al, , 1998; and the annelids Capitella teleta, , Meyer and Seaver, 2009, 2010, and Platynereis dumerilii, Ackerman et al, 2005Fischer and Arendt, 2013). Together, this body of work has revealed that the ultimate fates of these quadrants are, to a large extent, homologous across the embryos of different spiralian phyla.…”

Section: (B) Though All Four Macromeres Are Capable Of Becoming 3dmentioning

confidence: 99%

“…In many cases 2d also exhibits and early bilaterally symmetric pattern of cell divisions (Dohle, 1999). In the snail Crepidula 4d is the first cell to divide bilaterally to form the ML (left side) and MR (right side) mesendodermal teloblasts well before any of the other fourth quartet micromeres are even born (i.e., 4a, 4b and 4c, see Lyons et al, 2012). These teloblasts form bilaterally symmetrical bands of mesendodermal cells (see Lyons et al, 2012).…”

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confidence: 99%

“…In the snail Crepidula 4d is the first cell to divide bilaterally to form the ML (left side) and MR (right side) mesendodermal teloblasts well before any of the other fourth quartet micromeres are even born (i.e., 4a, 4b and 4c, see Lyons et al, 2012). These teloblasts form bilaterally symmetrical bands of mesendodermal cells (see Lyons et al, 2012). These cells also appear to generate the primordial germ cells in all cases in which this has been carefully examined (see reviewed by Rebscher, 2014 in this issue).…”

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confidence: 99%

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Spiralian model systems

Henry¹

2014

Int. J. Dev. Biol.

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The "Spiralia" represent one of the three major clades of bilaterian metazoans. Though members of this clade exhibit tremendous diversity in terms of their larval and adult body plans, many share a highly conserved early pattern of development involving a stereotypic cleavage program referred to as spiral cleavage. This group therefore represents an excellent one in which to undertake comparative studies to understand the origins of such diversity from a seemingly common ground plan. These organisms also present varied and diverse modes in terms of their ecology, development and life history strategies. A number of well established and emerging model systems have been developed to undertake studies at the molecular, genetic, cell and organismal levels. The Special Issue of the Int. J. Dev. Biol. entitled "Spiralian Model Systems" focuses on these organisms and here, I introduce this clade, pointing out different types of studies being undertaken with representative spiralian model systems. KEY WORDS: bilaterian metazoan, spiral cleavage, life history strategyThe Spiralia (Lophotrochozoa)Of the three major clades of bilaterians, the Spiralia (Lophotrochozoa) comprise nearly half of the extant metazoan phyla (see Fig. 1). Despite this fact, the group has received relatively little attention compared to the other two clades, the deuterostomes and ecdysozoans, notably in the areas of genetics, as well as molecular, cellular and developmental biology. This is due in part to the long standing predominance of key experimental models positioned within the Ecdysozoa, (e.g., the fruit fly Drosophila and the nematode, C. elegans), and the Deuterostomia, (e.g., chordates such as the Zebrafish and mouse, as well as a few invertebrate representatives from the Echinodermata).The Spiralia include 14 of roughly 36 metazoan phyla (Fig. 1). The Spiralia include the Lophotrochozoa, and sometimes these terms have been used synonomously. The clade "Lophotrochozoa" was first recognized by Halanych et al., (1995, see also Giribet et al., 2007 Helmkampf et al., 2008a,b;Dunn et al., 2008;Hejnol et al., 2009; Edgecomb et al., 2011) who showed that the Lophophorata (consisting of groups possessing characteristic ciliated feeding structures, such as brachiopods and phoronids), are clearly united with other protostome phyla that include annelids, molluscs, and nemerteans. The Spiralia, however, encompass an even larger group of metazoans, and the exact relationships amongst the Spiralia are, however, not fully resolved. The consensus from recent analyses suggest that there are two large sub-groups (clades). One group is the "Trochozoa," (Roule, 1891), which include Annelida, Int. J. Dev. Biol. 58: 389-401 (2014) doi: 10.1387/ijdb.140127jh Mollusca, Nemertea, as the "Eutrochozoa", together with the "Brachiozoa" (see Cavalier-Smith, 1998), comprised of Brachiopoda and Phoronida, and the "Polyzoa" (Funch and Kristensen 1995;Passamaneck and Halanych 2006; Helmkampf et al., 2008a,b;Edgecombe et al., 2011) consisting of the Bryozoa, E...

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“…Furthermore, the situation we observed is in agreement with classical descriptions on mesoderm formation and differentiation of solenogasters and polyplacophorans (Pruvot, 1890, 1892; Heath, 1899; Naef, 1924; Hammarsten and Runnström, 1925; Baba, 1938; Thompson, 1960; Salvini‐Plawen and Bartolomaeus, 1995) but is demonstrated here for the first time over the entire course of development using state‐of‐the‐art techniques. This suggests that the aculiferan mollusks have retained the plesiomorphic state of extensive and long‐lived mesodermal bands, and that the ephemeral and often rudimentary mesodermal bands are a derived condition of conchiferans (e.g., Patten, 1886; Lillie, 1895; Conklin, 1897; Wierzejski, 1905; Smith, 1935; Okada, 1936 1939; ’Crofts, 1937; Hinman and Degnan, 2002; Le Gouar et al., 2003; Lyons et al., 2012). …”

Section: Discussionmentioning

confidence: 99%

Cell Proliferation Pattern and Twist Expression in an Aplacophoran Mollusk Argue Against Segmented Ancestry of Mollusca

et al. 2016

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The study of aplacophoran mollusks (i.e., Solenogastres or Neomeniomorpha and Caudofoveata or Chaetodermomorpha) has traditionally been regarded as crucial for reconstructing the morphology of the last common ancestor of the Mollusca. Since their proposed close relatives, the Polyplacophora, show a distinct seriality in certain organ systems, the aplacophorans are also in the focus of attention with regard to the question of a potential segmented ancestry of mollusks. To contribute to this question, we investigated cell proliferation patterns and the expression of the twist ortholog during larval development in solenogasters. In advanced to late larvae, during the outgrowth of the trunk, a pair of longitudinal bands of proliferating cells is found subepithelially in a lateral to ventrolateral position. These bands elongate during subsequent development as the trunk grows longer. Likewise, expression of twist occurs in two laterally positioned, subepithelial longitudinal stripes in advanced larvae. Both, the pattern of proliferating cells and the expression domain of twist demonstrate the existence of extensive and long‐lived mesodermal bands in a worm‐shaped aculiferan, a situation which is similar to annelids but in stark contrast to conchiferans, where the mesodermal bands are usually rudimentary and ephemeral. Yet, in contrast to annelids, neither the bands of proliferating cells nor the twist expression domain show a separation into distinct serial subunits, which clearly argues against a segmented ancestry of mollusks. Furthermore, the lack of twist expression during the development of the ventromedian muscle argues against homology of a ventromedian longitudinal muscle in protostomes with the notochord of chordates.

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Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Cited by 68 publications

References 90 publications

The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella

The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella

Spiralian model systems

Cell Proliferation Pattern and Twist Expression in an Aplacophoran Mollusk Argue Against Segmented Ancestry of Mollusca

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