A biflagellate spermatozoon in the African bonytongue Heterotis niloticus (Teleostei, Osteoglossidae)

Abstract

In this transmission electron microscopy study, we describe the ultrastructure of the spermatozoon of Heterotis niloticus (Osteoglossiformes), which is distinguished by having two flagella. Our investigation also highlights the great diversity of sperm cell structures observed across osteoglossiform families, such as aflagellate (Gymnarchidae, Mormyridae), monoflagellate (Notopteridae, Pantodontidae) and biflagellate spermatozoa. As biflagellate spermatozoa are rare in vertebrates, we also summarize the orders and families known to possess this ultrastructural character, most of which are fishes.

Spermatogenesis in the inseminating African butterflyfish Pantodon buchholzi (Teleostei: Osteoglossiformes: Pantodontidae) with the revision of residual bodies formation

“…Unfortunately, lack of any studies on spermiogenesis in other osteoglossomorphs precludes the determination of whether they were producing flagellate or aflagellate aquasperm. Until now, the ultrastructure of flagellate spermatozoa is known only for H. niloticus, where biflagellate spermatozoa possess two cytoplasmic canals (Mattei et al ., 2019), and P. afer where Mattei (1970) indicated that a cytoplasmic canal is absent. Spermatozoa lacking a cytoplasmic canal were described in several species of Pimelodidae (Siluriformes): Pimelodus maculatus (Lacepède 1803), Pimelodus ornatus (Kner 1858), Pseudoplatystoma fasciatum L. and Sorubim lima (Bloch & Schneider 1801) (Batlouni et al ., 2006; Quagio Grassiotto & Carvalho, 2000; Quagio‐Grassiotto & Oliveira, 2008), and in the type of spermatogenesis designated as type III in which nuclear rotation does not occur and the flagellum is formed just posterior to the basal body and becomes associated with the plasma membrane.…”

“…Unfortunately, lack of any studies on spermiogenesis in other osteoglossomorphs precludes the determination of whether they were producing flagellate or aflagellate aquasperm. Until now, the ultrastructure of flagellate spermatozoa is known only for H. niloticus, where biflagellate spermatozoa possess two cytoplasmic canals (Mattei et al, 2019), and P. afer where Mattei (1970) (Mattei et al, 1967(Mattei et al, , 1972. A similar variation in terms of sperm structure (and possibly types of spermiogenesis) has appeared only in Myctophiformes (Neoteleostei, Scopelomorpha), which show both uniflagellate and biflagellate spermatozoa in some species (Hara, 2007;Hara & Okiyama, 1998;Mattei & Mattei, 1976;Ribes et al, 2015) and aflagellate spermatozoa in two species, Lampanyctodes hectoris (Günther 1876) and Diaphus danae (Tåning 1932) (Young et al, 1987).…”

“…The sole representative of the Pantodontidae, Pantodon buchholzi (Peters 1876), exhibits complex introsperm ultrastructure and sperm packet formation (Dymek & Pecio, 2019;van Deurs, 1975;van Deurs & Lastein, 1973), whereas all other osteoglossomorphs studied produce aquasperm. Uniflagellate aquasperm were reported only in the notopterid Papyrocranus afer (Günther 1868) (Mattei, 1970), and biflagellate aquasperm were described recently in the osteoglossid Heterotis niloticus (Cuvier 1829) (Mattei et al, 2019).…”

“…As Mattei et al . (2019) report, the only two groups of teleost fishes demonstrating examples of all the aforementioned sperm types are Myctophiformes and Osteoglossomorpha, a basal group of Osteoglossocephalai (Teleostei) (Betancur et al ., 2017). Among 272 extant osteoglossomorph species, sperm ultrastructure was investigated in 9 representatives of the families: Pantodontidae, Osteoglossidae, Notopteridae, Mormyridae and Gymnarchidae.…”

“…The sole representative of the Pantodontidae, Pantodon buchholzi (Peters 1876), exhibits complex introsperm ultrastructure and sperm packet formation (Dymek & Pecio, 2019; van Deurs, 1975; van Deurs & Lastein, 1973), whereas all other osteoglossomorphs studied produce aquasperm. Uniflagellate aquasperm were reported only in the notopterid Papyrocranus afer (Günther 1868) (Mattei, 1970), and biflagellate aquasperm were described recently in the osteoglossid Heterotis niloticus (Cuvier 1829) (Mattei et al ., 2019). Aflagellate spermatozoa, the most unique type in teleost fishes, are known for Gymnarchus niloticus (Cuvier 1829) (Mattei et al ., 1967) and five species of Mormyridae: Brienomyrus niger (Günther 1866), Marcusenius senegalensis L., Hyperopisus bebe (Lacepède 1803), Mormyrus rume (Valenciennes 1847) and Petrocephalus bovei (Valenciennes 1847) (Mattei, 1991; Mattei et al ., 1967, 1972).…”