Comparison of spermiogenesis in the externally fertilizing Hemigrammus erythrozonus and the inseminating Corynopoma riisei (Teleostei: Characiformes: Characidae)

Abstract

Spermiogenesis and sperm ultrastructure were analyzed in two species of characids with different modes of fertilization: externally fertilizing Hemigrammus erythrozonus and inseminating Corynopoma riisei. Spermiogenesis in H. erythrozonus is characterized by lateral development of the flagellum, nuclear rotation, formation of a shallow nuclear fossa, condensation of the chromatin by elimination of the electron-lucent area from the peripheral region of the nucleus, and renewal of the nuclear membrane. Multilammelated membrane and multivesicular bodies were also observed during elimination of the excess cytoplasm. The spermatozoon exhibits characters typical of "aquasperm," i.e. a spherical head containing a spherical nucleus with highly condensed chromatin, several small mitochondria located at the base of the nucleus within a cytoplasmic collar that extends into a long cytoplasmic sleeve surrounding the anterior part of the single flagellum, which is contained within a cytoplasmic canal. The flagellum lacks fins. The proximal and distal centrioles are nearly parallel to one another, with the anterior tips of both located within shallow nuclear fossae. Spermiogenesis in C. riisei is characterized by nuclear elongation alongside the forming flagellum, formation of an elongate cytoplasmic canal, displacement and elongation of the mitochondria, and uniform condensation of chromatin throughout the nucleus through enlargement of the diameter of the chromatin granules. The spermatozoon has an elongate nucleus with two elongate mitochondria localized to one side. Mitochondria are also located posterior to the nucleus forming a mitochondrial region. The single flagellum, which lacks fins, is lateral to the nucleus and initially contained within the greatly elongate cytoplasmic canal before exiting the canal at its posterior terminus. The spermatozoon of C. riisei exhibits several characters typical of "introsperm," such as an elongate nucleus and midpiece (mitochondrial region). The nuclear chromatin in the spermatozoon remains "flocculent" and is never as condensed as that seen in many characid sperm. Differences in spermiogenesis between externally fertilizing and inseminating characids are discussed.Foram analisadas a espermiogênese e ultraestrutura dos espermatozóides de dois caracídeos com modos de fertilização distintos: fertilização externa em Hemigrammus erythrozonus e inseminação em Corynopoma riisei. A espermiogênese em H. erythrozonus é caracterizada pelo desenvolvimento lateral do flagelo, rotação nuclear, formação de uma fossa nuclear rasa, condensação de cromatina por eliminação da área elétron-lúcida na região periférica do núcleo e renovação da membrana nuclear. Membrana multilamelada e corpos multivesiculares foram observados durante a eliminação do excesso de citoplasma. O espermatozóide exibe os caracteres típicos do "aquaespermatozóide," com uma cabeça esférica que contem um núcleo esférico com cromatina muito condensada, várias mitocôndrias pequenas localizadas na base do núcleo e dentro de um colar ...

Spermiogenesis and spermatozoa ultrastructure in the Serrasalminae (Ostariophysi: Characiformes) with further evidence on the relationships of the piranhas and pacus

“…In this case, the flagellum is eccentric to the nuclear axis, and the spermatozoa are of an intermediate type between types I and II (Mattei, 1970). Among the external fertilizing Characiformes, spermatozoa of the type I is the dominant type (Jamieson, 1991;Matos et al, 1993Matos et al, , 1998Burns et al, 1998;Magalhães, 1998;Romagosa et al, 1999;Aires et al, 2000;Zaiden, 2000;Andrade et al, 2001;Quagio-Grassiotto et al, 2001aAmaral, 2003;Cruz-Landim et al, 2003;Pecio, 2003;Azevedo, 2004;Weitzman et al, 2005;Veríssimo-Silveira et al, 2006;Oliveira, 2007;Pecio et al, 2007;Veríssimo-Silveira, 2007).…”

“…and Phenacogrammus interruptus, two derived taxa within the family Alestidae (see Zanata & Vari, 2005), the nucleus contain highly condensed, homogeneous granular chromatin (Veríssimo-Silveira, 2007), that may indicate later modifications of the chromatin in the evolution of derived taxa in Alestidae. Flocculent chromatin is also found in some inseminating species of the subfamily Stevardiinae (Pecio & Rafinski, 1999;Burns et al, 1998;Pecio et al, 2007).…”

“…Spermiogenesis and spermatozoa types, organell distribution and other particularities of the spermatic structure, have been found to be highly conservative in a given lineage at family or subfamily level, making them useful for phylogenetic analysis (Baccetti et al, 1984;Jamieson, 1991;Mattei, 1991;Burns et al, 1998;Quagio-Grassiotto et al, 2003). Regarding the Characiformes, and particularly the Characidae, the available information is still scarce considering the large diversity of the group (Jamieson, 1991;Matos et al, 1993Matos et al, , 1998Matos et al, , 2000Burns et al, 1998;Magalhães, 1998;Pecio & Rafinski, 1999;Romagosa et al, 1999;Aires et al, 2000;Zaiden, 2000;Andrade et al, 2001;Quagio-Grassiotto et al, 2001aAmaral, 2003;Cruz-Landim et al, 2003;Pecio, 2003;Azevedo, 2004;Pecio et al, 2005Pecio et al, , 2007Weitzman et al, 2005;Veríssimo-Silveira et al, 2006).…”

Spermatic characteristics and sperm evolution on the subfamily Stevardiinae (Ostariophysi: Characiformes: Characidae)

“…The resulting spermatozoa are referred to as Type I spermatozoa. However, among the Characiformes, incertae sedis in Characidae, spermiogenesis of the Type I with a complete nuclear rotation has to date been reported only in Hemigrammus erythrozonus (Pecio et al, 2007). Nuclear rotation, however, may be incomplete.…”

“…(Burns et al, 2009), Corynopoma riisei (Pecio et al, 2007), Mimagoniates barberi (Pecio & Rafiñski, 1999), Mimagoniates microlepis (Burns et al, 1998), Gephyrocharax atracaudata, Gephyrocharax intermedius (Burns et al, 2009), Pseudocorynopoma doriae (Burns et al, 1998), Tyttocharax cochui, Tyttocharax tambopatensis, Scopaeocharax rhinodus…”