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Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation

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Abstract

The tadpole stage of tunicates has played a pivotal role in understanding chordate evolution. While the organization of the mesoderm has been given high importance in comparative anatomical studies of Bilateria, this morphological character remains largely unexplored in tunicate tadpoles. For larvae of the phlebobranch ascidian Ciona intestinalis, the presence of two mesodermal pockets had been claimed, raising the possibility that paired coelomes are present in the larval ascidian. Using computer assisted 3D-reconstructions based on complete series of 1 μm-sections analyzed by light microscopy complemented by TEM-investigation of selected regions a comparative anatomical study of tadpole stages from four major tunicate clades, Aplousobranchiata, Phlebobranchiata, Stolidobranchiata, and Appendicularia is presented. In the aplousobranch Clavelina lepadiformis numerous mesodermal cells are found throughout the entire trunk plus the unpaired ventral rudiment of the pericardium. In the phlebobranch Ascidia interrupta, massive mesodermal components occur in the posterior trunk, whereas more anteriorly situated mesoderm consists of loose streaks of cells or isolated cells. This is also the case in the stolidobranch ascidians Herdmania momus and Styela plicata. In the stolidobranch Molgula occidentalis and the appendicularian Oikopleura dioica the anterior trunk is entirely devoid of mesodermal cells. TEM-investigation revealed that all mesodermal structures in the trunk of tunicate tadpoles were mesenchymal with the exception of a ventral portion of the mesoderm in C. lepadiformis, which probably corresponds to the developing pericardium, and the differentiated pericardium of the juvenile O. dioica. Thus no evidence for paired coelomic cavities in Tunicata was found. Outgroup comparison suggests that the reduction of paired coelomic cavities is an apomorphic trait of Tunicata. Within Tunicata a stepwise evolutionary reduction of the anterior larval mesenchyme is documented.

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References

  • Ax P (2001) Das System der Metazoa: ein Lehrbuch der phylogenetischen Systematik. Spektrum Akademischer Verlag GmbH, Heidelberg

    Google Scholar 

  • Barrington EJW (1965) The biology of hemichordata and protochordata. Oliver & Boyd, Edinburgh

    Google Scholar 

  • Bateson W (1885) The later stages in the development of Balanoglossus kowalevskyi, with a suggestion on the affinities of the Enteropneusta. Q J Microsc Sci 25:81–128

    Google Scholar 

  • Berrill NJ (1935) Studies in tunicate development. Part III—differential retardation and acceleration. Philos Trans R Soc Lond B 225:255–326. doi:10.1098/rstb.1935.0013

    Article  Google Scholar 

  • Burdon-Jones C (1952) Development and biology of the larva of Saccoglossus horsti (Enteropneusta). Philos Trans R Soc Lond B 236:553–589. doi:10.1098/rstb.1952.0010

    Article  Google Scholar 

  • Burighel P, Cloney RA (1997) Urochordata: Ascidiacea. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates. Hemichordata, chaetognathaand the invertebrate chordates. Willey, New York, pp 241–347

    Google Scholar 

  • Burighel P, Nunzi MG, Schiaffino S (1977) A comparative study of the organization of the sarcotubular system in ascidian muscle. J Morphol 153:205–224. doi:10.1002/jmor.1051530204

    Article  PubMed  CAS  Google Scholar 

  • Conklin EG (1905) Organization and cell lineage of the ascidian egg. J Acad Nat Sci Philadelphia 2nd Ser. XIII: 1–119, plates I-XII

  • de Pinna MCC (1991) Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367–394. doi:10.1111/j.1096-0031.1991.tb00045.x

    Article  Google Scholar 

  • de Sélys-Longchamps M (1939) Origine des premières ébauches cardiaques chez les Tuniciers. Trav Stat Zool Wimereux 13:629–634

    Google Scholar 

  • Davidson B, Levine M (2003) Evolutionary origins of the vertebrate heart: specification of the cardiac lineage in Ciona intestinalis. Proc Natl Acad Sci USA 100:11469–11473. doi:10.1073/pnas.1634991100

    Article  PubMed  CAS  Google Scholar 

  • Dohle W (2004) Die Verwandtschaftsbeziehungen der Großgruppen der Deuterostomier: alternative Hypothesen und ihre Begründung. Sitzungsber Ges Naturf Fr Berl 43:123–162

    Google Scholar 

  • Flood PR (1968) Structure of the segmental trunk muscle in amphioxus. Z Zellforsch 84:389–416. doi:10.1007/BF00334754

    Article  PubMed  CAS  Google Scholar 

  • Franz V (1925) Morphologische und ontogenetische Akranierstudien über Darm, Trichter, Zölomderivate, Muskulatur- und Bindegewebsformationen. Jenaische Zeitschr Naturwiss 61:407–468

    Google Scholar 

  • Gruhl A, Grobe P, Bartolomaeus T (2005) Fine structure of the epistome in Phoronis ovalis: significance for the coelomatic organization in Phoronida. Invertebr Biol 124:332–343. doi:10.1111/j.1744-7410.2005.00031.x

    Article  Google Scholar 

  • Hennig W (1984) Taschenbuch der speziellen Zoologie. Teil 1. Wirbellose 1. Verlag Harri, Deutsch

    Google Scholar 

  • Hirakow R (1989) Origin and differentiation of the chordate heart. In: Hilgers S (ed) Trends in vertebrate morphology. Gustav Fischer Verlag, Stuttgart, pp 261–263

    Google Scholar 

  • Hyman LH (1951) Introduction to the bilateria. McGraw-Hill, New York

    Google Scholar 

  • Jenner RA (2004) Towards a phylogeny of the Metazoa: evaluating alternative phylogenetic positions of Platyhelminthes, Nemertea, and Gnathostomulida, with a critical reappraisal of cladistic characters. Contrib Zool 73:3–163

    Google Scholar 

  • Jenner RA (2006) Challenging received wisdoms: some contributions of the new microscopy to the new animal phylogeny. Integr Comp Biol 46:93–103. doi:10.1093/icb/icj014

    Article  Google Scholar 

  • Katz MJ (1983) Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biol Bull 164:1–27. doi:10.2307/1541186

    Article  Google Scholar 

  • Kowalevsky A (1866) Entwickelungsgeschichte der einfachen Ascidien. Mémoires de l’Académie Impériale des Sciences de St-Pétersbourg VIIe Série: 1–19, 13 plates

  • Lohmann H (1956) Erste Klasse der Tunicaten. Appendiculariae. In: Krumbach T (ed) Handbuch der Zoologie. Walter de Gruyter, New York, pp 15–201

    Google Scholar 

  • Lüter C (2000) The origin of the coelom in Brachiopoda and its phylogenetic significance. Zoomorphology 120:15–28. doi:10.1007/s004359900019

    Article  Google Scholar 

  • Marcus E (1958) On the evolution of animal phyla. Q Rev Biol 33:24–58. doi:10.1086/402207

    Article  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: `mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474. doi:10.1242/dev.01119

    Article  PubMed  CAS  Google Scholar 

  • Masterman AT (1898) On the theory of archimeric segmentation and its bearing upon the phyletic classification of the Coelomata. Proc R Soc Edinb 22:270–310

    Google Scholar 

  • Mathysse AG, Deschet K, Williams M, Marry M, White AR, Smith WC (2004) A functional cellulose synthase from ascidian epidermis. Proc Natl Acad Sci USA 101:986–991. doi:10.1073/pnas.0303623101

    Article  Google Scholar 

  • Morgan TH (1894) The development of Balanoglossus. J Morphol 9:1–74. doi:10.1002/jmor.1050090102

    Article  Google Scholar 

  • Munro EG, Odell GM (2002) Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord. Development 129:13–24

    PubMed  CAS  Google Scholar 

  • Nakashima K, Yamada L, Satou Y, J-i Azuma, Satoh N (2004) The evolutionary origin of animal cellulose synthase. Dev Genes Evol 214:81–88. doi:10.1007/s00427-003-0379-8

    Article  PubMed  CAS  Google Scholar 

  • Nielsen C (1997) Tail evolution. Science 277:1422. doi:10.1126/science.277.5331.1421b

    Article  CAS  Google Scholar 

  • Nielsen C (2001) Animal Evolution. Interrelationships of the living phyla. Oxford University Press, New York

    Google Scholar 

  • Nishino A, Satoh N (2001) The simple tail of chordates: phylogenetic significance of appendicularians. Genesis 29:36–45. doi:10.1002/1526-968X(200101)29:1<36::AID-GENE1003>3.0.CO;2-J

    Article  PubMed  CAS  Google Scholar 

  • Oliphant LW, Cavey MJ (1972) The ascidian myocardium: sarcoplasmic reticulum and excitation-contraction coupling. Cell Tissue Res 129:395–412. doi:10.1007/BF00307296

    CAS  Google Scholar 

  • Pampapathi Rao K (1953) The development of Glandiceps (Enteropneusta: Spengelidae). J Morphol 93:1–17. doi:10.1002/jmor.1050930102

    Article  Google Scholar 

  • Remane A (1950) Entstehung der Metamerie der Wirbellosen. Zool Anz 14:16–23

    Google Scholar 

  • Romer AS, Parsons TS (1986) The vertebrate body. Saunders College, Philadelphia

    Google Scholar 

  • Ruppert EE (1997a) Cephalochordata (Acrania). In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates Hemichordata, Chaetognatha, and the invertebrate chordates. Wiley, New York, pp 349–504

    Google Scholar 

  • Ruppert EE (1997b) Introduction: microscopic anatomy of the notochord, heterochrony, and chordate evolution. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates hemichordata, chaetognatha, and the invertebrate chordates. Willey, New York, pp 1–13

    Google Scholar 

  • Salvini-Plawen Lv (1982) A paedomorphic origin of the oligomeric animals? Zool Scr 11:77–81. doi:10.1111/j.1463-6409.1982.tb00519.x

    Article  Google Scholar 

  • Scaal M, Wiegreffe C (2006) Somite compartments in anamniotes. Anat Embryol (Berl) 211:9–19. doi:10.1007/s00429-006-0127-8

    Google Scholar 

  • Schiaffino S, Grazia Nunzi M, Burighel P (1976) T system in ascidian muscle: organisation of the sarcotubular sytem in the caudal muscle cells of Botryllus schlosseri tadpole larvae. Tissue Cell 8:101–110. doi:10.1016/0040-8166(76)90023-9

    Article  PubMed  CAS  Google Scholar 

  • Seipel K, Schmid V (2006) Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 50:589–599. doi:10.1387/ijdb.062150ks

    Article  PubMed  Google Scholar 

  • Spring J, Yanze N, Josch C, Middel AM, Winninger B, Schmid V (2002) Conservation of brachyury, mef2, and snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. Dev Biol 244:372–384. doi:10.1006/dbio.2002.0616

    Article  PubMed  CAS  Google Scholar 

  • Stach T (1998) Coelomic cavities may function as a vascular system in amphioxus larvae. Biol Bull 195:260–263. doi:10.2307/1543137

    Article  Google Scholar 

  • Stach T (2000) Microscopic anatomy of developmental stages of Branchiostoma lanceolatum (Cephalochordata, Chordata). Bonner zool Monogr 47:1–111

    Google Scholar 

  • Stach T (2002) Minireview: on the homology of the protocoel in Cephalochordata and ‘lower’ Deuterostomia. A Zool (Stockholm) 83:25–31

    Article  Google Scholar 

  • Stach T (2007) Ontogeny of the appendicularian Oikopleura dioica (Tunicata, Chordata) reveals characters similar to ascidian larvae with sessile adults. Zoomorphology: 203-214. doi:10.1007/s00435-007-0041-5

  • Stach (2008) Chordate phylogeny and evolution: a not so simple three-taxon problem. J Zool (in press)

  • Stach T, Kirbach A (2008) Larval convergence in a colonial tunicate—the organization of the sarcotubular complex in Ecteinascidia turbinata (Perophoridae, Phlebobranchiata, Tunicata, Chordata). Zoomorphology (in press)

  • Stach T, Winter J, Bouquet J-M, Chourrout D, Schnabel R (2008) Evolution of life-cycles: the embryology of a planktonic tunicate reveals traces of sessility. Proc Natl Acad Sci USA 105:7229–7234. doi:10.1073/pnas.0710196105

    Article  PubMed  CAS  Google Scholar 

  • Starck D (1982) Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage. Band 3: Organe des aktiven Bewegungsapparates, der Koordination, der Umweltbeziehung, des Stoffwechsels und der Fortpflanzung. Springer, Berlin

    Google Scholar 

  • Strathmann RR, Staver JM, Hoffman JR (2002) Risk and the evolution of cell-cycle duration of embryos. Evolution 56:708–720

    PubMed  Google Scholar 

  • Swalla BJ (1993) Mechanisms of gastrulation and tail formation in ascidians. Microsc Res Tech 26:274–284. doi:10.1002/jemt.1070260403

    Article  PubMed  CAS  Google Scholar 

  • Technau U (2001) Brachyury, the blastopore and the evolution of the mesoderm. Bioessays 23:788–794. doi:10.1002/bies.1114

    Article  PubMed  CAS  Google Scholar 

  • Technau U, Scholz CB (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47:531–539

    PubMed  Google Scholar 

  • van der Horst CJ (1939) Hemichordata. Akademische Verlagsgesellschaft m. b. H, Leipzig

    Google Scholar 

  • von Ubisch L (1913) Die Entwicklung von Strongylocentrotus lividus (Echinus microtuberculatus, Arbacia pustulosa). Zeitschr wissensch Zool 106:409–448

    Google Scholar 

Download references

Acknowledgments

I want to thank A. Paasch, J. Winter, and C. Peschel for their help with the 3D-reconstructions. This study was supported through grants STA 655/1&2 from the German Science Foundation (Deutsche Forschungsgemeinschaft, DFG).

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Stach, T.G. Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation. Zoomorphology 128, 97–109 (2009). https://doi.org/10.1007/s00435-008-0076-2

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