Sperm and spermatozeugma ultrastructure in the inseminating speciesTyttocharax cochui,T. tambopatensis, andScopaeocharax rhinodus (Pisces: Teleostei: Characidae: Glandulocaudinae: Xenurobryconini)

Abstract

This article presents the scanning and transmission electron microscopy of the spermatozoa and sperm packets of three inseminating species of the glandulocaudine tribe Xenurobryconini. All three species, Scopaeocharax rhinodus, Tyttocharax cochui, and T. tambopatensis produce unencapsulated sperm packets (= spermatozeugmata) of similar morphology. The external anterior surface of each spermatozeugma is comprised of elongate sperm heads arranged in parallel, and the posterior part is made up of tightly packed flagella. The interior of the anterior portion consists of alternating layers of sperm heads and flagella. The remarkable integrity of each packet appears to be maintained through an electron-dense secretion seen among all parts of the cells. Spermatozeugma formation takes place within the spermatocysts at the end of spermiogenesis and at spermiation fully formed packets are released. Morphology of the mature spermatozoa was similar in all three species. Each nucleus is elongate, flattened along most of its length, and tapers at either end. The two centrioles are nearly parallel to one another and are located just anterior to the nucleus. Elongate mitochondria are located along the nucleus. The single flagellum, which lacks axonemal fins, is initially contained within a short cytoplasmic collar. Accessory microtubules run parallel to the long axis of the nucleus just beneath the plasma membrane. During spermiogenesis, no nuclear rotation occurs and the cytoplasmic canal containing the flagellum elongates along with the nucleus. However, prior to spermiation all but the anterior portion of the collar degenerates. The sperm modifications observed in these species are discussed as adaptations to the unique reproductive habit of insemination.

Reproductive morphology of Brittanichthys axelrodi (Teleostei: Characidae), a miniature inseminating fish from South America

“…However, it is the coiled posterior region that appears to be responsible for the final packaging of the sperm into distinct, unencapsulated packets (spermatozeugmata). In species of the subfamily Glandulocaudinae (sensu Weitzman et al, 2005), sperm packaging occurs within the posterior storage area (Pecio andRafiń ski, 1994, 1999;Burns et al, 1995;Pecio et al, 2001), whereas in those members of the subfamily Stevardiinae (sensu Weitzman et al, 2005) that produce spermatozeugmata, packaging takes place within the spermatocysts in the anterior spermatogenic region (Burns et al, 1995;Pecio et al, 2005). Sperm packaging may increase the probability of insemination by maintaining high sperm densities during transfer to the female (Ginzburg, 1968).…”

“…The sperm of the inseminating stevardiine characids Corynopoma riisei, Diapoma speculiferum, Scopaeocharax rhinodus, and Tyttocharax tambopatensis and the inseminating glandulocaudine Mimagoniates barberi also have elongate nuclei with flat surfaces (Burns et al, 1998;Pecio et al, 2005). Though elongate the sperm nuclei of inseminating cheirodontine characids (e.g., Compsura gorgonae) are more rounded in transverse section (Burns et al, 1997).…”

“…The long axes of centrioles may be parallel to one another as in Macropsobrycon uruguayanae , oblique as in Tyttocharax tambopatensis and Scopaeocharax rhinodus (Pecio et al, 2005), or perpendicular as in Diapoma (Burns et al, 1998), Pseudocorynopoma doriae , and Brittanichthys axelrodi. The functional significance of centriole arrangement is currently unclear.…”

“…Elongate binding collars containing flagella are found in mature spermatozoa of B. axelrodi, as well as the stevardiine genera Corynopoma, Diapoma, and Pseudocorynopoma (Burns et al, 1998) and Gephyrocharax and Chrysobrycon (unpublished data), and the cheirodontines Odontostilbe dialeptura and O. mitoptera (unpublished data). Elongate binding collars are present in the spermatids of the glandulocaudine genus Mimagoniates (Pecio andRafiń ski, 1994, 1999;unpublished data) and the stevardiine genera Tyttocharax and Scopaeocharax (Pecio et al, 2005); however, all but the anterior portions of the collars degenerate before the mature spermatozoa are released into the sperm ducts. The overall morphology and location of the mitochondria in B. axelrodi, mainly posterior to the nucleus, more closely resembles the condition observed in spermatozoa of inseminating cheirodontines (Burns et al, 1998; unpublished data) than in inseminating glandulocaudines and stevardiines, where mitochondria are found along the elongate nuclei (Pecio andRafiń ski, 1994, 1999;Burns et al, 1998;Burns and Weitzman, 2005).…”

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

“…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).…”