Ultrastructural study of spermatogenesis in Phoronopsis harmeri (Lophophorata, Phoronida)

Abstract

The process of sperm development in Phoronopsis harmeri was studied by electron microscopy. Developing spermatogenical cells are aggregated around the capillaries of the haemal plexus. The spermatogonia, which are situated around the capillary walls of the caeca, are remarkable for the presence of germ-line vesicles and contain their centrioles near the cell membrane. The spermatocytes and spermatids are flagellated cells arranged in clusters. During spermiogenesis the basal body/flagellum complex migrates to the apical pole of the spermatid. The acrosome-like structure arises from material produced by the Golgi complex. It lacks a surrounding membrane and has a fibrillar content. The nucleus elongates and the condensation of chromatin is caused by an activation of 'initiation centres'. The late spermatid and the spermatozoon appear as two-armed 'V'-shaped cells in which one arm contains the nucleus and posteriorly located mitochondria, and the other one is the axoneme. Spermatogenesis of P. harmeri is an interesting example of gamete differentiation where advanced sperm structure is combined with a plesiomorphic pattern of sperm development characterized as 'flagellate spermatogenesis'. Keywords Phoronopsis harmeri · Flagellate spermatogenesis · Spermatozoon IntroductionPresent ultrastructural investigations in Lophophorata (Tentaculata) allow a general view of mature sperm structure in representatives of all five sub-groups: Phoronida, Brachiopoda, Bryozoa, Entoprocta and Cycliophora (see Herrmann 1997;James 1997;Mukai et al. 1997;Nielsen and Jespersen 1997). However, the data on spermatogenesis are insufficient, as the complete process has so far been studied only in two species of brachiopods .Spermatozoa of Phoronida are typically 'V'-shaped (see Ikeda 1903;Cori 1939;Silen 1952;FranzØn 1956;Zimmer 1967;FranzØn and Ahlfors 1980;Herrmann 1997). In accordance with ultrastructural findings (FranzØn and Ahlfors 1980) one arm of the V contains the flagellum, and the other the nucleus and two elongated mitochondria. In Phoronis muelleri Selys-Longchamps, 1903 the spermatozoon has a needle-like acrosome, a short, almost round nucleus and a flagellum (Herrmann 1997). An ultrastructural study of phoronid sperm development has been carried out on Phoronis pallida Schneider, 1862 with a consideration of spermatid development only (FranzØn and Ahlfors 1980). The early stages of sperm development (spermatogonia and spermatocytes) have never been investigated in Phoronida. To fill this gap, spermatogenesis in Phoronopsis harmeri Pixell, 1912 has now been studied through all stages of sperm differentiation. MethodsSamples of Phoronopsis harmeri were collected in August 1996 in the intertidal zone of 'Vostok' Biological Station (Japan Sea, Russia). The species is gonochoristic (Zimmer 1967;Herrmann 1997). The males were identified by dissection and the gametes were observed using light microscopy.For the ultrastructural study the metasoma of three males were fixed in 2.5% glutaraldehyde in 0.1 M sodium cacodylate b...

Transition Zone Migration: A Mechanism for Cytoplasmic Ciliogenesis and Postaxonemal Centriole Elongation

“…(E) Distribution of spermatids containing either a centriolar midpiece or an axonemal midpiece across animal phylogeny. Based on (Afzelius, 1955; Al-Dokhi et al, 2007; Dallai et al, 1995; Dallai et al, 2010; Hess et al, 1991; Iomini and Justine, 1997; Lipke et al, 2009; Mattei, 1988; Medina, 1994; Mita and Nakamura, 1992; Reger and Cooper, 1968; Reunov and Klepal, 2003; Sato et al, 1967; Scheltinga et al, 2003; Silveira and Porter, 1964; Smita et al, 2004; Vignoli et al, 2008)…”

Problem of Terminology in Characteristics of Spermatozoa of Metazoa

“…8f). According to the authors who described the formation of male gametes in this species (Reunov and Klepal, 2004), the morphotype of modified spermatozoon is predominant, which forms during differentiation of the early spermatid. Displacement of the flagellum to the apically located aberrant acrosome-like structure (Fig.…”

“…The 9 + 2 formula of flagellum can be modified towards diverse combinations, which is explained by evolutionary regression of motile activity of spermatozoa in many invertebrates (Baccetti, 1984(Baccetti, , 1985. A full list of original structural features complementing the structure of Fregni et al, 1999); (c) Erpobdella octoculata (Hirudinea), TEM (after Garavaglia et al, 1974); (d-f) Phoronopsis harmeri (Phoronidae), SEM (d), TEM (e, f) (after Reunov and Klepal, 2004). 1, acrosome; 2, acrosome-like structure; 3, nucleus; 4, distal centriole-flagellum basal body; 5, flagellum; 6, mitochondrion.…”

Phoronida

“…How active internal sperm reach the ovary is one of the more intriguing aspects of phoronid biology. Even in species that are simultaneous hermaphrodites, self-fertilization has not been reported, as mature sperm released from the testes are not yet activated (Zimmer 1964 ;Reunov and Klepal 2004 ). Small masses of mature sperm released from the testes make their way through the trunk coelom until gathered up by the ciliary currents of the paired metanephridial funnels.…”

“…Primary oocytes are arrested at metaphase and released from the ovary to fuse with activated V-shaped sperm (Zimmer 1964(Zimmer , 1991Reunov and Klepal 2004 ). Male pronuclei have been found in the coelomic oocytes of Phoronopsis harmeri (Rattenbury 1953 ) and Phoronis ijimai (currently = vancouverensis ;Zimmer 1991 ;Hirose et al 2014 ).…”