Meiosis completion and various sperm responses lead to unisexual and sexual reproduction modes in one clone of polyploid Carassius gibelio

Abstract

Unisexual polyploid vertebrates are commonly known to reproduce by gynogenesis, parthenogenesis, or hybridogenesis. One clone of polyploid Carassius gibelio has been revealed to possess multiple modes of unisexual gynogenesis and sexual reproduction, but the cytological and developmental mechanisms have remained unknown. In this study, normal meiosis completion was firstly confirmed by spindle co-localization of β-tubulin and Spindlin. Moreover, three types of various nuclear events and development behaviors were revealed by DAPI staining and BrdU-incorporated immunofluorescence detection during the first mitosis in the fertilized eggs by three kinds of different sperms. They include normal sexual reproduction in response to sperm from the same clone male, typical unisexual gynogenesis in response to sperm from the male of another species Cyprinus carpio, and an unusual hybrid-similar development mode in response to sperm from another different clone male. Based on these findings, we have discussed cytological and developmental mechanisms on multiple reproduction modes in the polyploid fish, and highlighted evolutionary significance of meiosis completion and evolutionary consequences of reproduction mode diversity in polyploid vertebrates.

Molecular characterization and expression of an oocyte-specific histone stem-loop binding protein in Carassius gibelio

“…These examined tissues include heart, liver, spleen, kidney, muscle, hypothalamus, pituitary, ovary, and testis. embryogenesis (Gui and Zhu, 2012), slbp2 has almost identical expression pattern with spindlin (Sun et al, 2010;Zhang et al, 2015) and histone H2A variant h2af1o (Wu et al, 2009) during oogenesis and oocyte maturation of C. gibelio. They exhibit the highest expression at cortical alveolus stage, and their mRNAs and proteins also show similar intracellular localization in cytoplasm.…”

“…Up to now, however, no oocyte-specific SLBP have been characterized in fish. C. gibelio is a unique polyploid fish (Gui and Zhou, 2010;Jiang et al, 2013;Zhang et al, 2015) with dual reproduction modes of unisexual gynogenesis and sexual reproduction (Zhou et al, 2000;Mei and Gui, 2015). C. gibelio has become a promising model organism for understanding regulatory mechanisms of oocyte maturation, egg fertilization, and early embryogenesis (Gui and Zhou, 2010).…”

A novel allotetraploid gibel carp strain with maternal body type and growth superiority

“…Chromosome numbers of gibel carp were detected to range from 135 to 162 (Cherfas, 1981;Tóth et al, 2000;Liasko et al, 2010;Zhou and Gui, 2002;Kalous and Knytl, 2011), and its gynogenetic reproduction mode was preliminarily observed early in the last century (Golovinskaya et al, 1965;Peňáz et al, 1979). Later, through artificial propagation experiments, cytological investigation and molecular marker analyses, its dual reproduction modes were revealed, in which unisexual gynogenesis is resulted from heterologous sperm of other species and sexual reproduction is performed by homologous sperm from the males of same gibel carp clones (Gui and Zhou, 2010;Mei and Gui, 2015;Zhang et al, 2015). And, ploidy evolution was also reported to be still in the evolutionary progress (Murayama et al, 1986;Gui et al, 1993a;Liasko et al, 2010;Gui and Zhou, 2010;Zhang et al, 2015).…”

“…Gibel carp, also commonly known Prussian carp, which was previously nominated as a subspecies (Carassius auratus gibelio) (Fan and Shen, 1990;Gui, 1997), has been recently suggested as a separate species Carassius gibelio (Rylkova et al, 2010;Gui and Zhou, 2010;Kalous and Knytl, 2011;Wang et al, 2011;Zhang et al, 2015). It has been found throughout a vast territory of Eurasian continent (Kottelat and Freyhof, 2007;Jiang et al, 2013).…”

Molecular characterization and expression pattern of a germ cell marker gene dnd in gibel carp (Carassius gibelio)

“…However, unlike most unisexual vertebrates (Avise, 2008), gibel carp has been revealed to have multiple reproduction modes including unisexual gynogenesis and sexual reproduction (Zhou et al, 2000;Gui and Zhou, 2010;Li et al, 2014a;Mei and Gui, 2015;Zhang et al, 2015), and a high male incidence has been also observed in many natural populations (Jiang et al, 2013;Li et al, 2016). Utilizing it as an evolutional development biology model for screening reproduction-related genes, many important genes, such as oocytespecific and ovarian development-associated genes C-type lection (Dong et al, 2004), C1q-like (Mei et al, 2008(Mei et al, , 2014 and spindlin (Sun et al, 2010), oocyte-specific H2A variant h2af1o (Wu et al, 2009;Yue et al, 2013) and stem-loop binding protein-encoded gene slbp2 (Liu et al, 2015a), testis determination-related gene Dmrt1 (Li et al, 2014a), and germ cell marker genes Vasa and Dazl (Xu et al, 2005;Peng et al, 2009), have been identified and functionally characterized in gibel carp.…”