PhD thesis - Biologisk Institut - Københavns Universitet

Sipunculans and segmentationdevelopment, the ventral nerve cords fuseand the paired perikarya migrate towardseach other, resulting in two cell clusters offive cells each, which are grouped aroundthe now single ventral nerve cord (Fig. 2B).This results in loss of the metameric neuralpattern and eventually in the establishmentof the non-segmented ventral nervoussystem with only one single nerve cord. 18Noticeably, within Sipuncula the degreeof preservation of neural segmentationappears to be dependent on the duration ofthe larval phase and is thus directly correlatedwith the basal versus the derived modeof sipunculan development. The segmentednervous system in Phascolosoma is expressedin the so-called pelagosphera larva. Thislarval stage is a defining (apomorphic)character for Sipuncula and is thus consideredpart of the ancestral sipunculan lifecycle. 19 Neurogenesis in another sipunculanspecies that lacks the pelagospherastage, Phascolion strombi, shows that theremnants of the metameric nervous systemhave been reduced even further. As such,while also having a primarily paired ventralnerve cord, this species lacks the associatedperikarya and only has retained threetransitional ventral commissures as the soleremnants of the ancestral segmented neuralbodyplan. 20Cryptic segmentation in taxa withclose annelid affinities seems to be morecommon than previously assumed. Theechiurans (spoon worms), now consideredas clustering within Annelida, 13,16,17 donot show any segmental traits in their adultgross morphology. However, neurogenesisrevealed the same ontogenetic mechanismsas found in annelids and sipunculans, namely that paired sets ofperikarya are formed in a discrete anterior-posterior progression. 9-11In contrast to the sipunculans and similar to the condition foundin “typical” annelids, this metameric organization of the nervoussystem persists in the adult echiurans. Accordingly, the annelid-echiuran-sipunculanlineage shows a gradual decrease of preservationof nervous system segmentation, a notion that is further supportedby patterns of myogenesis. Hereby, annelids exhibit the typicalanterior-posterior progression of ring and dorsoventral muscleformation, while sipunculan myogenesis starts with synchronousformation of early ring muscle rudiments, followed by the emergenceof additional ring muscles along the entire anterior-posterioraxis by fission from already existing myocytes. 8,20 Accordingly,Sipuncula represents a developmental mosaic of segmental andnon-segmental bodyplan patterning mechanisms, whereby theectoderm-derived nervous system has to some degree maintainedits segmental ancestry while the mesodermal musculature is formedentirely non-metamerically.Figure 1. Schematic representation of neurogenesis in the polychaete annelid Sabellaria alveolata basedon serotonin immunoreactivity, revealing differences in the mode of establishment of metamery in theperipheral segmental neurons and the ventral commissures, respectively. Both aspects are ventral viewswith anterior facing upwards. Total length of the specimens is approximately 280 μm in (A) and 330μm in (B). (A) Late larva with synchronously established peripheral segmental neurons (yellow). Ventralcommissures and perikarya along the paired ventral nerve cord (vnc) are still lacking. The prototrochnerve ring (pnr) and the nerve ring underlying the telotroch (ttn) constitute subsets of the larval nervoussystem, while the circumoesophageal commissures (cc) and the longitudinal trunk neurons (ltn) are partsof the adult neural bodyplan. (B) Larva prior to metamorphosis. The ventral commissures (asterisks) ofthe first five segments have been established progressively, together with the paired, metameric sets ofperikarya (red dots) along the ventral nerve cords (vnc). The six pairs of peripheral segmental neurons(yellow) correspond to the segments II–VII, because development of segment I is retarded in this species,resulting in development of the paired peripheral segmental neuron of this segment at a later stage. Notethat ontogeny of the peripheral segmental neurons precedes development of the ventral commissures insegments VI and VII. pns – the nerves of the peripheral nervous system.Plasticity of SegmentationDespite the long standing definitions concerning the characteristicsof a segmented bodyplan (see above), recent data haveshown that the ontogenetic establishment of annelid segmentationmay follow quite different developmental pathways. Traditionally,it had been proposed that the first three (larval) segments formmore or less synchronously by schizocoely from the paired lateralmesodermal band, while the following (adult) segments developfrom a pre-anal growth zone. 21 Accordingly, one would assume thatthe organ systems associated with the first three segments also arisesynchronously, while only the subsequent segmental organs followthe anterior-posterior differentiation gradient. However, this is onlypartly true for the polychaete Sabellaria alveolata. While the threelarval segments indeed arise synchronously in this species, only thecorresponding pairs of peripheral segmental neurons form synchronously,while the ventral commissures develop subsequently oneafter another (Fig. 1). 22 While this may be interpreted as (secondary)www.landesbioscience.com Communicative & Integrative Biology 57