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

Abstract

The monophyly and phylogenetic relationships among the members of Clade A characids (sensu Malabarba & Weitzman), later redefined and named as the Stevardiinae (sensu Mirande), have been primarily supported by traditional morphological and molecular data. Herein were examined, described and compared spermiogenesis and sperm ultrastructure of 12 species of the genera Boehlkea, Bryconacidnus, Bryconamericus, Creagrutus, Cyanocharax, Hemibrycon, Knodus, Odontostoechus, Piabina, and Rhinobrycon in order to evaluate possible phylogenetic signals and their potential use in recovering relationships of the Stevardiinae. All examined species demonstrated a nuclear rotation equal or less than 95º resulting in a lateral position of the double nuclear fossa and flagellum. In all species, sperm nuclei are slightly elongate toward the flagellum, the proximal centriole is partially inside the nuclear fossa and lies anterior and oblique to the distal centriole, and the midpiece is short and strongly asymmetric. All species analyzed herein and other species previously examined for these systems in the Stevardiinae share homologous sperm characteristics as evidenced by spermiogenesis, further supporting the monophyly of this clade. Spermatozoa of the Stevardiinae further show three morphotypes (M1, M2, M3) of arrangement of centrioles, flagellum, nucleus and midpiece, hypothesized as successively derived in a series of transformation from the most basal morphotype (M1).A monofilia e filogenia dos membros do Clado A (sensu Malabarba & Weitzman), mais tarde redefinido e nomeado Stevardiinae (sensu Mirande), é suportada por dados morfológicos e moleculares. Aqui são examinadas, descritas e comparadas a espermiogênese e ultraestrutura do espermatozoide de 12 espécies dos gêneros Boehlkea, Bryconacidnus, Bryconamericus, Creagrutus, Cyanocharax, Hemibrycon, Knodus, Odontostoechus, Piabina e Rhinobrycon, a fim de avaliar possíveis sinais filogenéticos e seu uso potencial no estudo de relações filogenéticas em Stevardiinae. Em todas as espécies examinadas observa-se uma rotação nuclear igual ou menor que 95º, resultando em uma posição lateral da fossa nuclear dupla e do flagelo. Em todas as espécies o núcleo do espermatozoide é alongado em direção ao flagelo, o centríolo proximal é anterior e oblíquo ao centríolo distal e localiza-se parcialmente inserido na fossa nuclear, e a peça intermediária é pequena e fortemente assimétrica. Todas as espécies de Stevardiinae analisadas aqui e outras analisadas previamente compartilham características homólogas dos espermatozoides evidenciadas por sua espermiogênese, corroborando a monofilia deste clado. Os espermatozoides de Stevardiinae apresentam ainda três morfotipos (M1, M2, M3) de acordo com o arranjo dos centríolos, flagelo e peça intermediária, considerados como sucessivamente derivados em uma série de transformações a partir do morfotipo mais basal (M1).

Ontogenetic changes in mouth morphology triggers conflicting hypotheses of relationships in characid fishes (Ostariophysi: Characiformes)

“…This hypothesis was corroborated by molecular (Javonillo et al, 2010;Oliveira et al, 2011) and morphological (Mirande, 2010) phylogenies that support the monophyly of Clade A. Mirande (2010) named that clade Stevardiinae, which was further corroborated by Baicere-Silva et al (2011), who found that the spermiogenesis process in Odontostoechus lethostigmus is homologous with regard to other Stevardiinae.…”

Markiana nigripinnis (Perugia, 1891) as a putative member of the subfamily Stevardiinae (Characiformes: Characidae): spermatic evidence

“…Hypotheses based on exhaustive examination of characters using phylogenetic methodology that include the genus Markiana are largely limited to unpublished Ph.D. theses (Lucena, 1993;Benine, 2004;Moreira, 2007). Mirande (2010) Examination of the overall morphology of the spermatozoa of M. nigripinnis revealed similarities with the morphological pattern of the spermatozoa of the noninseminating members of Stevardiinae (Baicere-Silva et al, 2011). For an effective comparison, we accordingly describe the ultrastructural features of the spermatozoa of M. nigripinnis and present a discussion on its phylogenetic relationship.…”

Sperm ultrastructure in three different families of weakly electric fishes (Teleostei: Gymnotiformes)

“…Another type of spermiogenesis, type III, was described by Quagio-Grassiotto & Oliveira (2008), where the flagellum develops at a central position in relation to the nucleus, the nucleus does not rotate during spermiogenesis, and formation of a nuclear fossa and cytoplasmatic canal does not occur. Spermiogenesis type III is described for species of the family Pimelodidae (Quagio-Grassiotto & Oliveira, 2008;Quagio-Grassiotto & Carvalho, 2000), for some species of Callichthyidae e Loricariidae (Spadella, 2004), and for many species of the family Characidae (Baicere-Silva et al, 2011). Eigenmannia trilineata and the three Brachyhypopomus species analyzed all resemble type I spermatozoa, the most common type among Teleostei (Mattei, 1970), which is also observed in most species of Characiformes (QuagioGrassiotto et al, 2003;Burns et al, 2009), Cypriniformes (Bacceti et al, 1984Burns et al, 2009) and Siluriformes (Poirer & Nicholson, 1982;Burns et al, 2009) studied to date.…”

“…For this reason, results from sperm ultrastructure have provided valuable information on cellular modifications associated with reproductive habits and uncovered morphological characters useful in hypothesizing phylogenetic relationships (Baccetti, 1987;Baicere-Silva et al, 2011;Burns et al, 1998;Burns et al, 2002).…”