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Musculature in Sipunculan Worms: Ontogeny and Ancestral States

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Musculature in Sipunculan Worms: Ontogeny and Ancestral States EVOLUTION & DEVELOPMENT 11:1, 97–108 (2009) DOI: 10.1111/j.1525-142X.2008.00306.x Musculature in sipunculan worms: ontogeny and ancestral states Anja Schulzeà and Mary E. Rice Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, FL 34949, USA ÃAuthor for correspondence (email: [email protected]). Present address: Department of Marine Biology, Texas A & M University at Galveston, 5007 Avenue U, Galveston, TX 77551, USA. SUMMARY Molecular phylogenetics suggests that the introvert retractor muscles as adults, go through devel- Sipuncula fall into the Annelida, although they are mor- opmental stages with four retractor muscles that are phologically very distinct and lack segmentation. To under- eventually reduced to a lower number in the adult. The stand the evolutionary transformations from the annelid to the circular and sometimes the longitudinal body wall musculature sipunculan body plan, it is important to reconstruct the are split into bands that later transform into a smooth sheath. ancestral states within the respective clades at all life history Our ancestral state reconstructions suggest with nearly 100% stages. Here we reconstruct the ancestral states for the head/ probability that the ancestral sipunculan had four introvert introvert retractor muscles and the body wall musculature in retractor muscles, longitudinal body wall musculature in bands the Sipuncula using Bayesian statistics. In addition, we and circular body wall musculature arranged as a smooth describe the ontogenetic transformations of the two muscle sheath. Species with crawling larvae have more strongly systems in four sipunculan species with different de- developed body wall musculature than those with swimming velopmental modes, using F-actin staining with fluo- larvae. To interpret our findings in the context of annelid rescent-labeled phalloidin in conjunction with confocal laser evolution, a more solid phylogenetic framework is needed for scanning microscopy. All four species, which have smooth the entire group and more data on ontogenetic trans- body wall musculature and less than the full set of four formations of annelid musculature are desirable. INTRODUCTION roots of the respective clades. Whenever possible this should encompass all life history stages, because some stages may Sipuncula have long been regarded as a distinct protostome retain ancestral states more readily than others. This is ex- phylum (Hyman 1959; Stephen and Edmonds 1972; Cutler emplified in the Echiura, in which only the larvae retain a 1994). Most analyses have placed them in the lophotrochozoan segmented nervous system, indicative of their annelid origins clade (Zrzavy´et al. 1998; Giribet et al. 2000; Peterson and (Hessling and Westheide 2002). Ontogenetic transformations Ernisse 2001; Passamaneck and Halanych 2006), but until re- can also be informative characters themselves. cently relationships within the lophotrochozoans were largely In the Sipuncula, the body wall musculature and the in- unresolved. Today there is a growing consensus that sipuncul- trovert retractor muscles are important taxonomic characters. ans fall into the annelids (Boore and Staton 2002; Bleidorn The longitudinal and circular body wall muscles are either et al. 2005; Struck et al. 2007; Dunn et al. 2008), sparking a arranged in continuous sheaths or are broken up into nu- renewed interest in their morphology and development. merous bands. The number of introvert retractor muscles in As adults, their body is divided into a trunk and a re- the adults varies from one to four. They originate in the body tractable introvert with a crown of tentacles at its anterior wall of the trunk and insert in the head region. end, showing little resemblance to any known annelid group. Here we reconstruct the ancestral states of the two muscle More similarities to annelids are apparent in the larval stages, systems using Bayesian statistics. For this purpose, we rean- such as the trochophore larva with prototrochal and meta- alyze a simplified dataset of sipunculan sequence and mor- trochal ciliary bands, the retention of the egg envelope to phological data previously generated by the first author and form the larval cuticle and the paired ventral nerve cord in the collaborators (Schulze et al. 2007). In addition, we analyze pelagosphera larva of several species (Rice 1985). On the the ontogenetic transformations of the musculature using other hand, the absence of morphological segmentation in phalloidin-staining of F-actin and confocal laser scanning any life history stage is striking (Wanninger et al. 2005). microscopy. As these transformations may depend on the In general, to understand the morphological transforma- developmental mode of the species, we studied them in tions from one body plan to another, it is important to de- four sipunculan species displaying different developmental termine the ancestral states, that is character states at the patterns. & 2009 The Author(s) 97 Journal compilation & 2009 Wiley Periodicals, Inc. 98 EVOLUTION & DEVELOPMENT Vol. 11, No. 1, January^February 2009 I The head retractor muscles eventually transform into the in- trovert retractor muscles of the juvenile. The four species we chose for the present study all have less II than the full set of four introvert retractor muscles and con- tinuous layers of circular and longitudinal body wall muscu- lature. Phascolion cryptum (Fig. 2A) displays developmental III mode I (Rice 1975a). In the adult stage, a single introvert retractor muscle is present with two separate roots at the IV e a nc Fig. 1. The four developmental modes in the Sipuncula. I. Direct np development. II. Indirect development with a single pelagic stage, ir the lecithotrophic trochophore. III. Indirect development with a A lecithotrophic trochophore and a lecithotrophic pelagosphera. IV. Indirect development with a lecithotrophic trochophore and a planktotrophic pelagosphera. (Modified from Rice 1975a, b.) ee B Rice (1967, 1975a, b, 1976) describes four distinct develop- i mental patterns in the Sipuncula (Fig. 1): (1) direct develop- ment; (2) one pelagic larval stage: lecithotrophic trochophore; j (3) two pelagic larval stages: lecithotrophic trochophore and lecithotrophic pelagosphera; (4) two pelagic larval stages: le- cithotrophic trochophore and planktotrophic pelagosphera. The majority of sipunculan species of which development C has been studied, develop according to mode IV. The le- cithotrophic trochophore stage is generally short lived, but the pelagosphera may remain pelagic for 4–8 months (Scheltema and Hall 1975). Pelagosphera larvae swim by means of a dr strongly developed metatrochal ciliary band. When disturbed, vr their head region, including the metatroch, completely retracts into the trunk by a contraction of the head retractor muscles. D E Fig. 2. Developmental stages of Phascolion cryptum; (A) Introvert of adult emerging from gastropod shell, macrophotography; (B) Drawing of interior anatomy of adult; note single introvert retrac- tor muscle with two roots (arrows); (C) scanning electron micro- graph of juvenile in the process of elongation; 36 h post fertilization (p.f.); egg envelope still clearly visible in anterior part; (D–G) ju- venile stages, confocal laser scanning projections after fluorescent staining for F-actin with phalloidin Alexa 488. (D) Juvenile, 36 h p.f., dorsal slice. (E) Same specimen as (D), ventral slice. (F) Crawling stage, dorsal view, 3 days p.f.; note distinct bands of cm longitudinal and circular body wall musculature. (G) Same spec- vr imen, interior slice; note four head retractor muscles. a, anus; cm, circular body wall musculature; dr, dorsal head retractor muscles; dr e, esophagus; ee, egg envelope; ir, introvert retractor muscle; j, lm juvenile; lm, longitudinal body wall musculature; nc, nerve cord; F G np, nephridium; vr, ventral head retractor muscles. Scale bars: 20 mm. Schulze and Rice Myogenesis and phylogeny in sipuncula 99 posterior end of the trunk (Fig. 2B). Themiste lageniformis MATERIAL AND METHODS (Fig. 3A) develops according to mode III (Pilger 1987). Its pelagosphera larva is capable of swimming short distances but Ancestral state reconstruction Ancestral state reconstruction was performed by reanalyzing a spends most of its time crawling on the bottom. The adult has simplified version of the dataset first presented by Schulze et al. two introvert retractor muscles originating in the posterior (2007), with a constrained topology, using Bayesian statistics. The third of the trunk (Fig. 3B). Phascolion psammophilum (Fig. analysis included the same four gene regions (18S ribosomal RNA, 4A) also displays developmental mode III (Rice 1993a), but 28S ribosomal RNA, Histone H3, and cytochrome c oxidase sub- its pelagosphera larva is purely pelagic. As an adult, the spe- unit I) (Table 1) and 58 morphological characters and utilized the cies has a single large dorsal retractor muscle and a weaker same mixed models for the different data partitions. One difference ventral muscle with two separate roots (Fig. 4B). The fourth to the original analysis was that due to computing constraints only species, Nephasoma pellucidum (Fig. 5A) develops according 1,000,000 generations of Monte Carlo Markov chains were per- to mode IV (M. E. Rice, personal observation). It has two formed instead of 1,500,000. Of the 1,000,000 generations the initial introvert retractor muscles as an adult (Fig. 5B). 500,000 were discarded as burn-in. Another change from the pre- vious analysis was that for most species only
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