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

J Fish Biol. 2020 Nov;97(5):1491-1506. doi: 10.1111/jfb.14518. Epub 2020 Sep 17.

Abstract

The aim of this study was to analyse spermatogenesis in the African butterflyfish, Pantodon buchholzi, using transmission electron microscopy and scanning electron microscopy. P. buchholzi is the most basal teleost that exhibits insemination and produces a highly complex introsperm with the most elongate midpiece known in teleost fishes. Their early stages (spermatogonia and spermatocytes) do not differ greatly from those of other fishes, with the exception of Golgi apparatus degradation appearing as spindle-shaped bodies (SSBs). In round, early spermatids, the development of the flagellum begins after the migration of the centriolar complex towards the nucleus. Later, the elongation of the midpiece coincides with the displacement of the mitochondria and their fusion to produce nine mitochondrial derivatives (MDs). In these spermatids, the nucleus is situated laterally to the midpiece, with condensing chromatin in the centre of the nucleus. Within the midpiece, the flagellum is located within a cytoplasmic canal and is surrounded by a cytoplasmic sleeve containing fibres, MDs and a great amount of cytoplasm located on one side. During the next phase, nuclear rotation, the highly condensed chromatin is displaced to a position above the centriolar apparatus, whereas chromatin-free nucleoplasm is transferred to the cytoplasm. Later, this nucleoplasm, still surrounded by the nuclear membrane, is eliminated into the cyst lumen as the nucleoplasmic packet. Within the highly elongate spermatids, other excess organelles (SSBs, endoplasmic reticulum and mitochondria) are eliminated as residual bodies (RBs). Fully developed spermatozoa, which contain conical-shaped nuclei, eventually coalesce to form unencapsulated sperm packets (spermatozeugmata) that are surrounded by RBs at the level of the extremely elongate midpieces. Later, RBs are removed at the periphery of the cyst by means of phagocytosis by Sertoli cells.

Keywords: African butterflyfish; complex spermatozoon; residual bodies; spermatogenesis; spindle-shaped body.

MeSH terms

  • Animals
  • Cell Nucleus / ultrastructure
  • Cytoplasm / ultrastructure
  • Fishes / physiology*
  • Flagella / ultrastructure
  • Male
  • Microscopy, Electron, Scanning
  • Microscopy, Electron, Transmission
  • Mitochondria / ultrastructure
  • Spermatids / ultrastructure
  • Spermatocytes / ultrastructure
  • Spermatogenesis / physiology*
  • Spermatogonia / ultrastructure
  • Spermatozoa / ultrastructure*