Sipuncula: an emerging model of spiralian development and evolution

Abstract

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...

Re-evaluating the phylogeny of Sipuncula through transcriptomics

“…Within Sipuncula, there are four recognized life history patterns, including direct development, and indirect development with lecithotrophic and planktotrophic modes of larval formation (Rice, 1975(Rice, , 1976(Rice, , 1985Boyle and Rice, 2014). As with previous molecular hypotheses (e.g., Maxmen et al, 2003;Schulze et al, 2007;Kawauchi et al, 2012) our transcriptome analyses confirm Sipunculidae as the sister clade to all other sipunculans.…”

“…Third, sipunculans are valuable research organisms for reproductive biology (Rice, 1973(Rice, , 1989(Rice, , 1993Reunov and Rice, 1993;Adrianov and Maiorova, 2010), comparative development (Åkesson, 1958;Rice, 1967Rice, , 1975Rice, , 1988Schulze and Rice, 2009a) and life history character reconstruction and evolution (Jägersten, 1972;Rice, 1976Rice, , 1985. They are also emerging as important non-model organisms for evolutionary and developmental biology, or evo-devo (Schulze and Rice, 2009b;Wanninger et al, 2005Wanninger et al, , 2009Wanninger, 2008;Boyle and Seaver, 2010;Boyle and Rice, 2014). Fourth, due to an extended larval phase described for several species within multiple families Hall, 1965, 1975;Rice, 1976Rice, , 1981Scheltema and Rice, 1990), sipunculans constitute an interesting group for studying dispersal within and between widely separated oceanic regions, which is a topic addressed in several recent studies of cosmopolitanism in the marine realm (Staton and Rice, 1999;Kawauchi and Giribet, 2010;Kawauchi and Giribet, 2013;Schulze et al, 2012;Young et al, 2012;Lemer and Planes, 2014).…”

Ins and outs of Spiralian gastrulation

“…In the polychaete Capitella, and in the sipunculan Themiste, which both gastrulate by epiboly, foxA is expressed in the endoderm during gastrulation (Boyer and Seaver, 2008;, which is at odds with the hypothesis presented by Arenas-Mena (2013). Likewise, brachyury is expressed prior to gastrulation in vegetal macromeres in Capitella (Boyle and Rice, 2014). The expression patterns of genes such as brachyury and foxA have been reported in several species that exhibit "intermediate" forms of gastrulation.…”

“…Some studies have begun to ask if genes known to be necessary for normal gastrulation in other metazoans, for example the transcription factors brachyury and foxA (Kusch and Reuter, 1999;Fritzenwanker et al, 2004;Annunziata et al, 2014), could also be expressed during gastrulation stages in spiralians (ArenasMena, 2013;Boyle and Rice 2014). In the polychaete Hydroides, brachyury and foxA are expressed dynamically in the blastopore as cells invaginate (Arenas-Mena, 2006 Fig.…”

“…Furthermore, are particular genes associated with all ectomesoderm internalization? Unlike endomesoderm, which has an evolutionarily conserved gene regulatory network (e.g., Röttinger et al, 2012 , Boyle andRice, 2014), the factors regulating ectomesoderm remain to be uncovered, and might be very different between species.…”