Chapter III 52Chapter IIIWanninger A, Kristof A & Brinkmann N. 2009. Sipunculans andsegmentation. Communicative & Integrative Biology 2: 56-59
[Communicative & Integrative Biology 2:1, 56-59; January/February 2009]; ©2009 Sipunculans Landes Bioscience and segmentationMini-ReviewSipunculans and segmentationAndreas Wanninger,* Alen Kristof and Nora BrinkmannUniversity of Copenhagen; Department of Biology; Research Group for Comparative Zoology; Copenhagen, DenmarkKey words: Sipuncula, evolution, segmentation, seriality, annelid, Echiura, nervous system, development, phylogeny, bodyplanComparative molecular, developmental and morphogeneticanalyses show that the three major segmented animal groups—Lophotrochozoa, Ecdysozoa and Vertebrata—use a wide range ofontogenetic pathways to establish metameric body organization.Even in the life history of a single specimen, different mechanismsmay act on the level of gene expression, cell proliferation,tissue differentiation and organ system formation in individualsegments. Accordingly, in some polychaete annelids the first threepairs of segmental peripheral neurons arise synchronously, whilethe metameric commissures of the ventral nervous system form inanterior-posterior progression. Contrary to traditional belief, lossof segmentation may have occurred more often than commonlyassumed, as exemplified in the sipunculans, which show remnantsof segmentation in larval stages but are unsegmented as adults.The developmental plasticity and potential evolutionary lability ofsegmentation nourishes the controversy of a segmented bilaterianancestor versus multiple independent evolution of segmentation inrespective metazoan lineages.Ontogeny and Functional Implications of SegmentationThe evolution of a segmented bodyplan is often considered acrucial metazoan innovation because it allows the subdivision andspecialization of individual body regions along the anterior-posterioraxis of an animal. 1,2 This partitioning typically involves both theectodermal and the endodermal germ layers and often resultsin metameric ectodermal appendages (parapodia) and segmentallyarranged, paired mesodermal body cavities (coelomic sacs).Traditionally, a condition where all segments have the same typeof parapodia and house identical sets of internal organs such asganglia, nephridia, gonads and muscles has been regarded as basalfor annelids and arthropods (homonomic segmentation). 1,2 Fromthis basal (plesiomorphic) condition, concentration of individualorgan systems into segments of specific body regions combinedwith reductions of organs in other segments are thought to haveoccurred multiple times within various lineages, and eventually led tomorphologically distinct segments along the anterior-posterior bodyaxis (heteronomic segmentation). 1,2*Correspondence to: Andreas Wanninger; University of Copenhagen; Departmentof Biology; Research Group for Comparative Zoology; <strong>Universitet</strong>sparken 15;Copenhagen DK-2100 Denmark; Email: awanninger@bio.ku.dkSubmitted: 11/26/08; Accepted: 12/01/08Previously published online as a Communicative & Integrative Biology E-publication:http://www.landesbioscience.com/journals/cib/article/7505While often considered an important hint towards ancestralsegmentation of a species, serial repetition of organs along the anterior-posterioraxis alone is not decisive for a segmental evolutionaryhistory (cf., e.g., the multiple ring muscles in the non-segmentedplatyhelminths). On the cellular and organ system level, segmentationcan only be proven with the aid of developmental studies,because segmented animals typically exhibit a posterior growth zonefrom which all segments are progressively budded off. 3-7 Accordingly,ontogenetically older segments—and thus also the organs associatedwith them—are found anterior to the younger segments, a fact thatis illustrated by the gradual decrease of the degree of organ systemdifferentiation from anterior to posterior (Fig. 1). 8 This makes thepattern of organogenesis an ideal marker to test for the segmentalancestry of worm-shaped lophotrochozoan taxa. 8-12Coelomic compartmentalization of a cylindrical body hasfrequently been proposed to be of selective advantage due to the factthat these animals are able to regulate the hemolymphic pressure ineach compartment (segment) individually. The interplay of coelomicpressure and the contractile ring and longitudinal muscles of thebody wall enable direct and independent control over the diameterof the body in each individual segment, thus allowing for a diversityof complex movement patterns. 2 However, while coelomic segmentationhas often (but not always) been retained in large, burrowingannelids (e.g., earthworms), secondary loss is often observed in nonbenthicfree-living (e.g., leeches), interstitial (e.g., Protodrilus), orsessile forms (e.g., tube worms).Loss of SegmentationDespite the loss of segmentation in various annelid taxa, ontogeneticremnants of their segmented ancestry are present in a numberof annelids that do not show obvious segmental features in the adultbody (e.g., leeches). 3,4 Recent developmental studies have shownthat this holds also true for representatives of the Sipuncula (peanutworms), unsegmented lophotrochozoans that are regarded eitheras derived ingroup annelids or as a direct annelid sister clade. 13-17Interestingly, however, segmental traits in the sipunculans arerestricted to the nervous system but have been completely lost on thelevel of coelom organisation. 18 Accordingly, larvae of Phascolosomaagassizii develop four pairs of perikarya that are associated with thepaired ventral nerve cord and express the common neurotransmitterserotonin (Fig. 2A). These paired perikarya form, together withcommissures that interconnect the ventral nerve cords, in a typicalannelid-like anterior-posterior progression, thus demonstratingthe segmental ancestry of Sipuncula. During subsequent larval56 Communicative & Integrative Biology 2009; Vol. 2 Issue 1
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