PhD thesis - Biologisk Institut - Københavns Universitet

Sipunculans and segmentationFigure 2. Expression and loss of the segmental pattern of the ventral CNS in the sipunculan Phascolosomaagassizii, as depicted by 3D reconstruction of serotonin immunoreactivity. Both aspects are ventral viewswith anterior facing upwards. Total length of the specimens is approximately 150 μm. (A) Late larvawith four pairs of metameric perikarya (red; boxed area) associated with the ventral nerve cord (vnc).The latter is already fused along the entire anterior-posterior axis except in the anterior-most region.Additional neural elements include the cells of the larval apical organ (dark blue) overlying the neuropilmass (np) of the adult brain, the first cell bodies of the developing adult brain (light blue), two cells ofthe peripheral nervous system (orange), and the larval prototroch nerve ring (green). (B) Larva prior tometamorphosis in which the metameric arrangement of the ventral perikarya (red) has been lost in favorof two cell clusters (boxed areas) comprising five cells each. Note the increased number of cells belongingto the adult brain (light blue).chronological dissociation of larval segment formation and thedevelopment of the ventral commissures, it could alternatively beexplained as the result of a heterochronic shift of the first threesegments, which were originally derived from a posterior growthzone, into the larval stage of the animal. This notion is supportedby reports that describe an—albeit rapid—progressive formation ofthese first three pairs of coelomic sacs in several polychaete taxa. 23Whatever alternative holds true, this example demonstrates that thedevelopmental mechanisms that underlie annelid segmentation aremuch more complex than previously assumed. This is confirmed byrecent cell proliferation pattern analyses, which suggest that the locationof the growth zone might have shifted from a posterior-medianposition to both lateral sides in some species, indicating positionalvariability of the annelid growth zone. 24 However, despite the highmorphogenetic plasticity of segmentation, some molecular mechanismsappear similar even between distant phylogenetic entities suchas arthropods and vertebrates. 25,26Ancestry of SegmentationComparative analyses of the developmentalmechanisms that form metamericorgans in segmented lophotrochozoanworms demonstrate a high plasticityof ontogenetic patterns that lead to asegmented bodyplan and show thatsegmentation may be lost during evolution.This raises the question as to whatextent such an evolutionary loss has yetremained unrecognized in other phyla, thusreviving the discussion about a possiblesegmented ancestor of Lophotrochozoa andBilateria as a whole. Such a scenario hasbeen repeatedly proposed by the advocatesof a conserved molecular pathwaythat is thought to underlie the ontogenyof metazoan segmentation. 7,26 However,despite some similarities on the molecularlevel, there are also significant differencesin the way typical “segmentation genes” areexpressed, and cellular and tissue differentiationpathways that eventually give rise toindividual segments vary between lophotrochozoans,vertebrates and ecdysozoans. 25To complicate matters further, segmentformation is highly variable even betweenphyla within the respective “superclades”Ecdysozoa and Annelida. 25 Moreover,morphologically similar segments mayfollow different ontogenetic pathways evenwithin the same individual, and distinctmetamerically arranged subunits of thenervous system may form differently inindividual segments of the same animal(e.g., the ventral commissures versus theperipheral segmental neurons in polychaetes;see above). Lastly, a mosaic ofsegmental and non-segmental modes oforganogenesis may occur within an individual, indicating the occurrenceof dissociation of organogenesis from the segmentation processin some species (e.g., muscle formation in sipunculans; see above).Given the incongruencies and the plasticity of the processesinvolved in the ontogeny of segmentation in the various major bilateriansubgroups, no final statement as to whether or not Urbilateriawas segmented can yet be made. In any case, assuming a segmentedurbilaterian would imply a wide range of evolutionary modificationsof the ancestral segmentation pathway on the molecular, cellularand morphogenetic level, as well as secondary loss of a segmentedbody in a number of lineages. Both, experimental developmentalgenetics employing RNAi experiments and comparative morphogeneticanalyses provide exciting tools that enable us to directly test forevolutionary hypotheses concerning shared molecular segmentationpathways on the one hand and for cryptic remnants of a segmentedbodyplan in seemingly non-segmented recent phyla on the other.This should eventually lead to a sound reconstruction of the ancestry58 Communicative & Integrative Biology 2009; Vol. 2 Issue 1