Developmental Patterns in Spiralian Embryos

Hydroides elegans is an indirectly developing polychaete with equal spiral cleavage, gastrulation by invagination, and a feeding trochophore. Expression of several transcription factors and differentiation genes has been characterized. Comparative analysis reveals evolutionarily conserved roles. For example, the synexpression of transcription factors FoxA and Brachyury suggests homology of primary and secondary gut openings in protostomes and deuterostomes, and the expression of Sall suggests similar regulatory controls in the posterior growth zone of bilaterians. Differences in gene expression suggest regulatory differences control gastrulation by invagination in polychaetes with a feeding trochophore and gastrulation by epiboly in polychaetes without a feeding trochophore. Association of histone variant H2A.Z with transcriptional potency and its expression suggest a developmental role during both embryogenesis and the larva-to-adult transformation. Methods are being developed for experimental exploration of the gene regulatory networks involved in trochophore development in Hydroides. It is unknown if polychaete feeding trochophores evolved from a larval stage already present in the life cycle of the last common ancestor of protostomes and deuterostomes. Previous evolutionary scenarios about larval origins overemphasize the discontinuity between larval and adult development and require the early evolution of undifferentiated and transcriptionally potent "set aside" cells. Indirect development may proceed by developmental remodeling of differentiated cells and could have evolved after gradual transformation of juveniles into larvae; undifferentiated and transcriptionally potent cells would have evolved secondarily. Comprehensive characterization of gene regulatory networks for feeding trochophore development may help resolve these major evolutionary questions. KEY WORDS: bilaterian, posterior growth, serpulid, annelidHydroides elegans, a polychaete with a feeding trochophore Characterization of polychaetes with a feeding trochophore, such as Hydroides elegans ( Fig. 1 and Table 1), is relevant to understand the developmental evolution of complex life cycles in spiralians. Embryonic development in polychaetes conforms to the presence or absence of a feeding trochophore (Fig. 2). In the genus Hydroides (Eupomatus), embryogenesis ends in a feeding trochophore endowed with an equatorial ciliary band, a protonephridium, various sensory organs, and a functional gut formed after gastrulation by invagination (Hatschek, 1885;Shearer, 1911). Blastomeres 4d and 2d22 are inconspicuous and fated to contribute to the mesodermal and ectodermal portions of the segmented body that will have primarily a reproductive role; the Int. J. Dev. Biol. 58: 575-583 (2014) growth and proliferation of 4d and 2d22 are feeding-dependent. In contrast, during embryogenesis in polychaetes without feeding larvae, blastomeres 4d and 2d are relatively large and immediately engage in the formation of segments (Fig. 2). In addition to la...

Section: Spiral -Sinistral-equal Cleavage In Hydroides and Early Genesupporting

confidence: 54%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

“…1 Sipunculan models of spiralian development 487 Boyer and Henry, 1998;Hejnol, 2010;Lambert, 2010). And new forms of evidence from understudied taxa will likely confirm why spiral cleavage is viewed as a flexible character complex that builds diverse larval and adult body plans (Henry and Martindale, 1999;Hejnol, 2010).…”

Section: Ancient Worms With a New Statusmentioning

confidence: 98%

“…The 4d cell divides to produce a pair of teloblasts that will form bands of mesoderm (Hatschek, 1883;Gerould, 1906), presumably homologous to endomesoderm in other spiralians where cell lineage/fate studies have been performed. A polar lobe has not been detected, and it is not known when or how the D quadrant is established or if there is a sipunculan organizer, although a combination of unequal cleavage and conspicuously large D macromere suggest the mechanism may be similar to what is implicated in mollusk and polychaete embryos (Clement, 1962;Henry and Martindale, 1999;Henry, 2002;Lambert, 2007Lambert, , 2010.No cell-lineage experiments by injection of intracellular tracers have been performed in a sipunculan embryo, and therefore direct cellfate characterizations in embryos or later stages are unavailable. Gastrulation in sipunculans occurs by epiboly with lecithotrophic development, and by invagination and/or epiboly in species with planktotrophic development (Hatschek, 1883;Åkesson, 1958;Rice, 1967;Rice, 1975b).…”

mentioning

confidence: 99%

“…In order to move this group of spiralians forward as valuable comparative models, we will need to generate such data as demonstrated by intracellular fate-mapping studies (Boyer et al, 1996;Henry and Martindale, 1998;Maslakova et al, 2004;Hejnol et al, 2007;, and several next-generation sequencing projects Riesgo et al, 2012;Simakov et al, 2012;Lapraz et al, 2013). If successful, this would provide the basic information and technology to pursue comparative bioinformatics and functional genomics research (Newmark and Sanchez Alvarado, 2002;Lambert, 2010;Lambert et al, 2010). …”

mentioning

confidence: 99%

See 1 more Smart Citation

Sipuncula: an emerging model of spiralian development and evolution

Boyle¹,

Rice²

2014

Sipuncula is an ancient clade of unsegmented marine worms that develop through a conserved pattern of unequal quartet spiral cleavage. They exhibit putative character modifications, including conspicuously large first-quartet micromeres and prototroch cells, postoral metatroch with exclusive locomotory function, paired retractor muscles and terminal organ system, and a U-shaped digestive architecture with left-right asymmetric development. Four developmental life history patterns are recognized, and they have evolved a unique metazoan larval type, the pelagosphera. When compared with other quartet spiral-cleaving models, sipunculan development is understudied, challenging and typically absent from evolutionary interpretations of spiralian larval and adult body plan diversity. If spiral cleavage is appropriately viewed as a flexible character complex, then understudied clades and characters should be investigated. We are pursuing sipunculan models for modern molecular, genetic and cellular research on evolution of spiralian development. Protocols for whole mount gene expression studies are established in four species. Molecular labeling and confocal imaging techniques are operative from embryogenesis through larval development. Nextgeneration sequencing of developmental transcriptomes has been completed for two species with highly contrasting life history patterns, Phascolion cryptum (direct development) and Nephasoma pellucidum (indirect planktotrophy). Looking forward, we will attempt intracellular lineage tracing and fate-mapping studies in a proposed model sipunculan, Themiste lageniformis. Importantly, with the unsegmented Sipuncula now repositioned within the segmented Annelida, sipunculan worms have become timely and appropriate models for investigating the potential for flexibility in spiralian development, including segmentation. We briefly review previous studies, and discuss new observations on the spiralian character complex within Sipuncula. KEY WORDS: pelagosphera, metatroch, unequal, U-shaped, ectomesoderm Ancient worms with a new statusSipuncula is a clade of unsegmented, coelomate marine worms. They have colonized benthic habitats worldwide from intertidal zones to abyssal plains in polar, temperate and tropical environments, and they have evolved a larval form that is unique among all metazoans, the pelagosphera (Mueller, 1850;Hatschek, 1883;Gerould, 1906;Rice, 1967). The adult body plan consists of a relatively large posterior trunk region with a single undivided coelomic cavity, and a retractable introvert with an array of tentacles on the anterior end that typically surrounds the mouth. The mouth leads to a U-shaped digestive system that terminates with an anus on the dorsal-anterior side of the trunk. Adult sipunculans have a centralized nervous system with a single, median, unsegmented Int. J. Dev. Biol. 58: 485-499 (2014) doi: 10.1387/ijdb.140095mb ventral nerve cord. There is comprehensive information on their reproductive biology (Rice, 1975b;Rice, 1989), anatomy (Rice, 1973(R...

“…Spiral cleavage where the cleavage planes are at oblique angles to the animal-vegetal axis of the egg occurs during the second (or may be even the first?) to fifth cleavages in alternating rotation direction, but they are most notable during the third to fifth cleavages (Meshcheryakov, 1975;Verdonk and van den Biggelaar, 1983;Lambert, 2010). Embryos manually forced to rotate clockwise way at the third cleavage opposite to the wild type, underwent anticlockwise rotation first during the macromere division and then during the micromere division as well, in the subsequent fourth cleavage.…”

Section: B C D Amentioning

confidence: 99%

Spiral cleavages determine the left-right body plan by regulating Nodal pathway in monomorphic gastropods, Physa acuta

Abe¹,

Takahashi²,

Kuroda³

2014

The handedness of gastropods is genetically determined, but the molecular nature of the gene responsible and the associated mechanisms remain unknown. In order to characterize the chiromorphogenesis pathway starting from the gene to the left-right asymmetric body plan, we have closely analyzed the cytoskeletal dynamics of the Physa (P.) acuta embryo, a fresh water non-dimorphic sinistral snail, during the early developmental stage by mechanically altering the handedness of the embryos at the critical spiral third cleavage. A fertile situs inversus was created and the nodal-Pitx gene expression patterns were completely mirror imaged to the wild type at the trochophore stage. Together with our previous work on Lymnaea (L.) stagnalis, we could show that chirality is established at the third cleavage, as dictated by the single handedness-determining gene locus, and then chirality information is transferred via subsequent spiral fourth and fifth cleavages to the later developmental stage, dictating the nodal-Pitx expression pathway. The cytoskeletal dynamics of manipulated and non-manipulated embryos of sinistral P. acuta and dextral dominant L. stagnalis are compared.