Spermatogenesis inPyrosoma atlanticum (Tunicata: Thaliacea: Pyrosomatida): Implications for tunicate phylogeny

Abstract

Abstract. Colonies of Pyrosoma 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 35 #m long. The head is differentiated into a bulbous posterior portion 5 #m long x 1 #m wide, a thinner anterior portion 25 #m long tapering from a width of 0.7 #m to a width of 0.4 #m, and a very thin anterior extension 5 #m long x 0.5 #m 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 in P. 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.

Sessile lifestyle and origin of chordates

“…This derivation appears improbable as the doliolids are pelagic, selection pressure for the maintenance of a planktonic larva is diminished, and it seems unlikely that a neotenic organism could have arisen from a larval form in process of decline. Additionally, comparative sperm morphology does not support the view that doliolids gave rise to the larvaceans (Holland 1990). Results of ultrastructural studies on sperm and spermatogenesis are compatible with the belief that the four pelagic tunicate groups arose independently from ascidian-like predecessors (Holland 1989(Holland , 1990.…”

“…Additionally, comparative sperm morphology does not support the view that doliolids gave rise to the larvaceans (Holland 1990). Results of ultrastructural studies on sperm and spermatogenesis are compatible with the belief that the four pelagic tunicate groups arose independently from ascidian-like predecessors (Holland 1989(Holland , 1990. The sperm of the Larvacea among the pelagic groups display the most plesiomorphic (primitive) features; they contrast with those of other pelagic tunicates in having a compact, rounded rather than elongated head, a distinctly demarcated midpiece, and a fully functional acrosome .…”

“…Certain colonial animals in organic continuity, like single organisms, may have attained freedom from a permanently fixed condition, as suggested by Holland (1989Holland ( ,1990 for the doliolids and Pyrosoma. Progression of freed colonies with a benthic habit would present obvious difficulties, and colonies assumed to be secondarily released from a sessile state are characteristically floating forms (e.g., the doliolids, pyrosomes, salps, and the elaborate siphonophores).…”

Brachyury (T) gene expression and notochord development in Oikopleura longicauda (Appendicularia, Urochordata)

“…Nielsen 1995). Recently, several lines of evidence support the view that appendicularians represent the group that diversified earliest among the five distant classes of tunicates (Holland 1989(Holland , 1990Holland and Holland 1989;Wada and Satoh 1994;Wada 1998;Nishino et al 2000;Swalla et al 2000). These results imply that, in order to define the ancestral characters of chordate bodies, understanding the tailed body plan of appendicularians, which may be directly comparable to those of other chordates, is indispensable.…”

“…According to the recent morphological and molecular phylogenetic analyses, it is most likely that the ancestral stock of tunicates initially diverged the group of appendicularians (Haeckel 1868;Brooks 1893;Tokioka 1971;Holland and Holland 1989;Holland 1989Holland , 1990Wada and Satoh 1994;Wada 1998;Swalla et al 2000), although the analysis on the 18S rDNA data set indicated that the position of appendicularians leaves ambiguity because of the relatively high rate of genetic changes in their sequences Swalla et al 2000). Some studies have suggested the tailed freeswimming, not sessile, organism as the ancestor of tunicates (Wada 1998;Nishino et al 2000;Swalla et al 2000).…”