Abstract
Colonies ofPyrosoma atlanticum were collected by submersible in October 1988 in the Caribbean Sea, and testes were studied by electron microscopy. Spermatogonia, spermatocytes and early spermatids have two centrioles. The proximal centriole subsequently disappears, its remains apparently persisting in the spermatozoon as dense material adjacent to the distal centriole, which gives rise to the axoneme. At the tip of early spermatids are several 50 nm proacrosomal vesicles, which disappear leaving no trace in early elongating spermatids. The spermatozoon lacks an acrosome and has a head 35µm long. The head is differentiated into a bulbous posterior portion 5µm long × 1µm wide, a thinner anterior portion 25µm long tapering from a width of 0.7µm to a width of 0.4µm, and a very thin anterior extension 5µm long × 0.5µm wide. At the start of elongation, the anterior extension begins to form just lateral to the proacrosomal vesicles as a spiral projection comprising part of the nucleus, covered by a thin sheath of cytoplasm. This sheath of cytoplasm undergoes a complex differentiation. Ultimately, the nucleus in the anterior extension is overlain by two membrane-bound sheaths of cytoplasm connected by a spiral flange of cytoplasm. Between these two sheaths is a spiral space, open to the exterior through a subterminal pore near the sperm tip. In early spermatids the mitochondria fuse into a single mitochondrion, which remains lateral to the nucleus. The cristae become modified late in spermatogenesis. Throughout elongation of the spermatid there are patches of dense material between the nucleus and mitochondrion. A manchette of microtubules transiently encircles the thin anterior portion of the nucleus during the last phase of elongation. A manchette is not present during most of elongation. In the spermatozoon the mitochondrion, which has reticulate cristae, spirals a few times about the nucleus and extends from the junction between the bulbous portion and the thinner anterior portion of the nucleus to the junction between the thinner anterior portion and the nuclear extension. Spermatogenesis inP. atlanticum, compared to that in other tunicates, most closely resembles that in colonial ascidians, and supports the majority view that pyrosomes arose from aplousobranch ascidians that lost their attachment to the substratum. Pyrosome sperm are more highly derived than doliolid sperm, which have an acrosome that is probably capable of exocytosis. When salp and pyrosome sperm are compared, both are highly derived, but neither shares any apomorphies with the other that it does not share with at least one other tunicate order. Thus, sperm morphology does not support the majority view that pyrosomes gave rise to doliolids and neither confirms nor denies the idea that pyrosomes are intermediate between aplousobranch ascidians and salps. Therefore, it is likely that the class Thaliacea is polyphyletic, with doliolids arising very early from the ascidian lineage and with salps and pyrosomes arising somewhat later.
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Literature cited
Asa, C. S., Phillips, D. M. (1988). Nuclear shaping in spermatids of the Thai leaf frogMegaphrys montana. Anat. Rec. 220: 287–290
Balfour, F. M. (1885). A treatise on comparative embryology. 2nd ed. Vol. 2. MacMillan, London
Berrill, N. J. (1936). Studies in tunicate development. V. Evolution and classification. Phil. Trans. R. Soc. (Ser. B) 225: 43–70
Berrill, N. J. (1950). The Tunicata with an account of the British species. Ray Society, London
Brien, P. (1948). Embranchement des tuniciers. Traité Zool. 11: 553–894
Brooks, W. K. (1893). The genusSalpa. Mem. biol. Lab. Johns Hopkins Univ. 2: 1–396, 57 plates
Burighel, P., Martinucci, G. B., Magri, F. (1985). Unusual structures in the spermatozoa of the ascidiansLissoclinum perforatum andDiplosoma listerianum (Didemnidae). Cell Tissue Res. 241: 513–521
Cary, S. C., Felbeck, H., Holland, N. D. (1989). Observations on the reproductive biology of the hydrothermal vent tube wormRiftia pacyptilia. Mar. Ecol. Prog. Ser. 52: 89–94
Cloney, R. A., Abbott, L. C. (1980). The spermatozoa of ascidians: acrosome and nuclear envelope. Cell Tissue Res. 206: 261–270
Colwin, A. L., Colwin, L. H. (1955). Sperm entry and the acrosome filament (Holothuria atra andAsterias amurensis). J. Morph. 97: 543–567
Cotelli, R., De Santis, R., Rosati, F., Monroy, A. (1980). Acrosome differentiation in the spermatogenesis ofCiona intestinalis. Dev. Growth Differentiation 22: 561–569
Dan, J. C. (1952). Studies on the acrosome. I. Reaction to egg water and other stimuli. Biol. Bull. mar. Biol. Lab., Woods Hole 103: 54–66
Fawcett, D. W., Anderson, W. A., Phillips, D. M. (1971). Morphogenetic factors influencing the shape of the sperm head. Devl Biol. 26: 220–251
Fenaux, R. (1967). Les appendiculaires des mer d'Europe et du Bassin Méditerranéen. Faune Eur. Bassin méditerr. 2: 1–113
Field, K. G., Olsen, G. J., Giovannoni, S. J., Raff, E. C., Pace, N. R., Raff, R. A. (1989). Response to phylogeny and molecular data. Science, N.Y. 243: 550–551
Field, K. G., Olsen, G. J., Lane, D. J., Giovannoni, S. J., Ghiselin, M. T., Raff, E. C., Pace, N. R., Raff, R. A. (1988). Molecular phylogeny of the animal kingdom. Science. N.Y. 239: 748–753
Flood, P. R., Afzelius, B. A. (1978). The spermatozoon ofOikopleura dioica Fol (Larvacea, Tunicata). Cell Tissue Res. 191: 27–37
Franzén, Å. (1956). On spermiogenesis, morphology of the spermatozoon and biology of fertilization among invertebrates. Zool. Bidr. Upps. 31: 354–482
Franzén, Å. (1958). On sperm morphology and acrosome filament formation in some Annelida, Echiuroidea, and Tunicata. Zool. Bidr. Upps. 33: 1–28
Franzén, Å. (1970). Phylogenetic aspects of the morphology of spermatozoa and spermiogenesis. In: Baccetti, B. (ed.) Comparative spermatology. Academic Press, New York, p. 29–46
Franzén, Å. (1976). The fine structure of spermatid differentiation in a tunicateCorella parallogramma (Müller). ZOON 4: 115–120
Franzén, Å. (1983a). Urochordata. In: Adiyodi, K. G., Adiyodi, R. G. (eds.) Reproductive biology of invertebrates. Vol. 2. John Wiley & Sons, Chichester, p. 621–632
Franzén, Å. (1983b). Ultrastructural studies of spermatozoa in three bivalve species with notes on evolution of elongated sperm nucleus in primitive spermatozoa. Gamete Res. 7: 199–214
Fukumoto, M. (1979). Tube-like structures in mitochondria of tunicate (Pyura vittata). J. Ultrastruct. Res. 68: 1–5
Fukumoto, M. (1981). The spermatozoa and spermiogenesis ofPerophora formosana (Ascidia) with special reference to the striated apical structure and the filamentous structures in the mitochondrion. J. Ultrastruct. Res. 77: 37–53
Fukumoto, M. (1983). Fine structure and differentiation of the acrosome-like structure in the solitary ascidians,Pyura haustor andStyela plicata. Dev. Growth Differentiation 25: 503–515
Fukumoto, M. (1984a). Fertilization in ascidians: acrosome fragmentation inCiona intestinalis spermatozoa. J. Ultrastruct. Res. 87: 252–262
Fukumoto, M. (1984b). The apical structure inPerophora annectens (Tunicate) spermatozoa: fine structure, differentiation and possible role in fertilization. J. Cell Sci. 66: 175–187
Fukumoto, M. (1985). Acrosome differentiation inMolgula manhattensis (Ascidiacea, Tunicata). J. Ultrastruct. Res. 92: 158–166
Fukumoto, M. (1986). The acrosome in ascidians: Pleurogona. Int. J. Invertebrate Reprod. Dev. (Amsterdam) 10: 335–346
Fukumoto, M. (1988). Fertilization in ascidians: apical processes and gamete fusion inCiona intestinalis spermatozoa. J. Cell Sci. 89: 189–196
Fukumoto, M. (1989). The acrosome reaction inCiona intestinalis (Ascidia, Tunicata). Dev. Growth Differentiation 31: p. 397
Garstang, W. (1892). On the development of the stigmata in ascidians. Proc. R. Soc. 51: 505–513
Garstang, W. (1928). The morphology of the Tunicata, and its bearing on the phylogeny of the Chordata. Q. Jl microsc. Sci. 72: 51–187
Ghiselin, M. T. (1988). The origin of molluscs in the light of molecular evidence. Oxf. Surv. evolut. Biol. 5: 66–95
Godeaux, J. (1957–1958). Contribution à la connaisance des thaliacés (Pyrosoma etDoliolum). Annls Soc. r. zool. Belg. 88: 1–285
Grobben, D. (1882).Doliolum und sein Generationswechsel. Arb. zool. Inst. Univ. Wien 4: 201–298
Hawkins, C. J., Kott, P., Parry, D. L., Swinehart, J. H. (1983). Vanadium content and oxidation state related to ascidian phylogeny. Comp. Biochem. Physiol. 76B: 555–558
Heider, K. (1900). Tunicata. In: Korscheldt, E., Heider, K. (eds.) Textbook of the embryology of invertebrates. Sonnenschein, London, p. 334–534 [Translated from German by M. Bernard and M. W. Woodward]
Herdman, W. (1888). Report on the Tunicata collected by HMS Challenger during the years 1873–1876. Rep. scient. Results Voyage HMS Challenger (s: Zool.) 27: 1–57
Hodgson, A. N., Bernard, R. T. F. (1988). A comparison of the structure of the spermatozoa and spermatogenesis of 16 species of patellid limpet (Mollusca: Gastropoda: Archaeogastropoda). J. Morph. 195: 205–223
Holland, L. Z. (1988). Spermatogenesis in the salpsThalia democratica andCyclosalpa affinis (Tunicata: Thaliacea): an electron microscope study. J. Morph. 198: 189–204
Holland, L. Z. (1989). Fine structure of spermatids and sperm ofDolioletta gegenbauri andDoliolum nationalis (Tunicata: Thaliacea): implications for tunicate phylogeny. Mar. Biol. 101: 83–95
Holland, L. Z., Gorsky, G., Fenaux, R. (1988). Fertilization inOikopleura dioica (Tunicata: Appendicularia): acrosome reaction, cortical reaction and sperm-egg fusion. Zoomorphology 108: 229–243
Honegger, T. G. (1986). Fertilization in ascidians: studies on the egg envelope, sperm and gamete interactions inPhallusia mammillata. Devl Biol. 118: 118–128
Huxley, T. H. (1851). Observations upon the anatomy and physiology ofSalpa andPyrosoma, together with remarks uponDoliolum and Appendicularia. Phil. Trans. R. Soc. 1851(2): 457–605
Huxley, T. H. (1859). On the anatomy and development ofPyrosoma. Trans. Linn. Soc. Lond. 23: 193–250
Ihle, I. E. W. (1910). Die Thaliaceen (einschließlich Pyrosomen) der Siboga-Expedition. E. J. Brill, Leiden (Monographie 56 aus Uitkomsten op zoologisch, botanisch, oceanographisch en geologisch gebied verzameld in Nederlandsch Oost-Indie 1899–1900)
Jefferies, R. P. S. (1987). The ancestry of the vertebrates. British Museum (Natural History), London
Julin, C. (1896). Recherches sur la blastogenèse chezDistaplia magnilarva etD. rosea. In: Compte-rendu des séances du troisième congrès international de zoologic. E. J. Brill, Leyde, p. 507–524
Julin, C. (1904). Recherches sur la phylogenèse des tuniciers. Développement de l'appariel branchial. Z. wiss. Zool. 76: 544–611
Kessel, R. G. (1966). Electron microscope studies on the origin and maturation of yolk in oocytes of the tunicate,Ciona intestinalis. Z. Zellforsch. 71: 525–544
Kondo, T., Hasegawa, K., Uchida, T. Z. (1988). Formation of the microtubule bundle and helical shaping of the spermatid in the common finch,Lonchura striata var.domestica. J. Ultrastruct. molec. Struct. Res. 98: 158–168
Lohmann, J. (1933). Erster Unterstamm der Chordata. Tunicata = Manteltiere. Allgemeine Einleitung in die Naturgeschichte der Tunicata. Handb. Zool. 5(2): 3–14
Metcalf, M. M. (1918). The Salpidae: a taxonomic study. Bull. U.S. natn. Mus. 100 2(2): 1–193
Metcalf, M. M., Hopkins, H. S. (1919). Pyrosoma. A taxonomic study based upon the collections of the United States Bureau of Fisheries and the United States National Museum. Bull. U.S. natn. Mus. No. 100 2(3): 195–275
Neumann, G. (1933). Zweite Klasse der Tunicata. Acopa = Caducichordata. Erste Unterklasse der Acopa Thaliaceae. Handb. Zool. 5(2): 203–400
Oka, S. (1912). Eine neue phylogenetisch interessante Synascidie. (Cyathocormus mirabilis n.g. n.sp.). Zool. Anz. 40: 257–261
Penny, D. (1989). What, if anything, isProchloron? Nature, Lond. 337: 304–305
Phillips, D. M. (1976). Nuclear shaping during spermiogenesis in the whip scorpion. J. Ultrastruct. Res. 54: 397–405
Raff, R. A., Field, K. G., Ghiselin, M. T., Lane, D. J., Olsen, G. J., Pace, N. R., Parks, A. L., Parr, B. S., Raff, E. C. (1988). Molecular analysis of distant phylogenetic relationships in echinoderms. In: Paul, C. R. C., Smith, A. B. (eds.) Echinoderm phylogeny and evolutionary biology. Clarendon Press, Oxford, p. 29–41
Ritter, W. (1905). The pelagic Tunicata of the San Diego region, excepting the Larvacea. Univ. Calif. Publs Zool. 2: 51–112
Rosati, F., Pinto, M. R., Casazza, G. (1985). The acrosomal region of the spermatozoon ofCiona intestinalis: its relationship with the binding to the vitelline coat of the egg. Gamete Res. 11: 379–389
Salensky, W. (1893). Über die Entstehung der Metagenesis bei Tunicaten. Biol. Zbl. 13: 126–146
Seeliger, O. (1893–1911). Tunicata: Mantelthiere. Bronn's Kl. Ordn. Tierreichs 3 (Suppl): 1–1773
Van Soest, R. M. W. (1981). A monograph of the order Pyrosomatida (Tunicata, Thaliacea). J. Plankton Res. 3: 603–631
Theophiloff, S. (1892). Zur Phylogenie der Tunicaten. Eine kritische Studie. Inaugural-Dissertation der philosophischen Fakultät der Universität Jena zur Erlangung der philosophischen Doktorwürde. B. Engau, Jena
Tokioka, T. (1971). Phylogenetic speculation of the Tunicata. Publs Seto mar. biol. Lab. 19: 43–63
Tuzet, O., Bogoraze, D., Lafargue, F. (1972). Recherches ultrastructurales sur la spermiogenèse deDiplosoma listerianum (Milne-Edwards, 1841) etLissoclinum pseudoleptoclinum (Von Drasche, 1883) ascidies composées, aplousobranches. Annls Sci. nat. (sér. Zool.) (12e Sér). 14: 177–190
Tuzet, O., Bogoraze, D., Lafargue, F. (1974). La spermatogenèse dePolysynchraton lacazei, 1872 etTrididemnum cereum Giard (ascidies composées, aplousobranches). Bull. biol. Fr. Belg. 108: 151–167
Uljanin, B. (1884). Die Arten der GattungDoliolum im Golfe von Neapel und den angrenzenden Meeresabschnitten. Fauna Flora Golf. Neapel 10: 1–140
Villa, L. (1975). An ultrastructural investigation of normal and irradiated spermatozoa of a tunicate,Ascidia malaca. Boll. Zool. 42: 95–98
Villa, L. (1981). An electron microscope study of spermiogenesis and spermatozoa ofMolgula impura andStyela plicata (Ascidiacea, Tunicata). Acta Embryol. Morph. exp. (N.S.) 2: 69–85
Villa, L., Tripepi, S. (1983). An electron microscope study of spermatogenesis and spermatozoa ofAscidia malaca, Ascidiella aspersa andPhallusia mammillata (Ascidiacea, Tunicata). Acta Embryol. Morph. exp. (N.S.) 4: 157–168
Webster, P. M., Richards, S. K. (1977). Spermiogenesis in the enchytraeidLumbricillus rivalis (Oligochaeta: Annelida). J. Ultrastruct. Res. 61: 62–77
West, D. L. (1978). Ultrastructural and cytochemical aspects of spermiogenesis inHydra hymanae, with reference to factors involved in sperm head shaping. Devl Biol. 65: 139–154
Wirth, U. (1984). Die Struktur der metazoen Spermien und ihre Bedeutung für die Phylogenetik. Verh. naturw. Ver. Hamb. 27: 295–362
Young, J. Z. (1981). Life of the vertebrates. 3rd ed. Clarendon Press, Oxford, New York
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Communicated by M. G. Hadfield, Honolulu
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Holland, L.Z. Spermatogenesis inPyrosoma atlanticum (Tunicata: Thaliacea: Pyrosomatida): Implications for tunicate phylogeny. Mar. Biol. 105, 451–470 (1990). https://doi.org/10.1007/BF01316317
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DOI: https://doi.org/10.1007/BF01316317