A novel transient structure with phylogenetic implications found in ratite spermatids

Abstract

BackgroundA novel transient structure was observed in the spermatids of three ratite species using transmission electron microscopy.ResultsThe structure first appeared at the circular manchette stage of sperm development, was most prominent during the longitudinal manchette phase and disappeared abruptly prior to spermiation. It was composed of regularly-spaced finger-like projections which were closely associated with the outer nuclear membrane, giving the nucleus a cogwheel-like appearance. The projections were approximately 30 nm long and 14 nm wide. Although a similar structure has been described in certain lizard and crocodile species, this is the first report of a similar structure in the developing spermatids of birds.ConclusionsThe potential value of non-traditional characters, such as spermiogenesis and sperm ultrastructure, as phylogenetic markers has recently been advocated. The morphologically unique structure found in ratite spermatids provides additional evidence of a possible phylogenetic link between the reptiles and birds. It also endorses the basal positioning of the ratites as a monophyletic group within the avian phylogenetic tree.

Spermiogenesis in birds

“…Other non-mammalian vertebrates known to display a similar structure are crocodiles 117 and certain lizard species. [117][118][119][120][121][122][123][124][125][126] Du Plessis and Soley 115 view this as an additional evidence that reptiles and birds share a common ancestry, as has been previously suggested.…”

“…In the ratite, this structure appears when the LM is fully formed, and disappears just before spermiation. 115 Its function is not known, but these authors have discussed the significance of this finding, in ratite birds, with regard to phylogeny among birds. Other non-mammalian vertebrates known to display a similar structure are crocodiles 117 and certain lizard species.…”

“…Du Plessis and Soley 115 have described, for the first time, in late spermatids of birds, specifically of the emu, ostrich and rhea, a structure comprising regularly-spaced, finger-like projections that are immediately adjacent to the outer nuclear membrane (Fig. 9D, E).…”

Sperm head shaping in ratites: New insights, yet more questions

“…4d,e), although they were more prominent in the region immediately beneath the base of the acrosome. The morphological characteristics of the definitive form of the projections have previously been described in detail (Du Plessis and Soley, 2013). The mean length of the projections was 29.8 ± 4.2nm with a mean width at the base of 13.4 ± 2.5nm.…”

“…The possible involvement of a PT, or indeed the existence of this structure, has not been reported in birds, although the translucent layer beneath the forming acrosome and the peri-nuclear fibro-granular layer posterior to the acrosome (Aire, 2007(Aire, , 2014Fawcett et al, 1971) described in some species would suggest the existence of a PT in this vertebrate order. The recent identification of a unique, transient cytoplasmic structure that manifests during spermiogenesis around the post-acrosomal region of the sperm nucleus in ratites (Du Plessis and Soley, 2013) provides compelling evidence for the presence of an analogous entity, at least in ratites. This paper documents the morphological events relevant to head shaping that occur during spermiogenesis in three ratite species, the ostrich (Struthio camelus), emu (Dromaius novaehollandiae) and rhea (Rhea americana albisceus).…”