Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio

Abstract

A unisexual species is generally associated with polyploidy, and reproduced by a unisexual reproduction mode, such as gynogenesis, hybridogenesis or parthenogenesis. Compared with other unisexual and polyploid species, gibel carp (Carassius auratus gibelio) has a higher ploidy level of hexaploid. It has undergone several successive rounds of genome polyploidy, and experienced an additional, more recent genome duplication event. More significantly, the dual reproduction modes, including gynogenesis and sexual reproduction, have been demonstrated to coexist in the polyploid gibel carp. This article reviews the genetic basis concerning polyploidy origin, clonal diversity and dual reproduction modes, and outlines the progress in new variety breeding and gene identification involved in the reproduction and early development. The data suggests that gibel carp are under an evolutionary trajectory of diploidization. As a novel evolutionary developmental (Evo-Devo) biology model, this work highlights future perspectives about the functional divergence of duplicated genes and the sexual origin of vertebrate animals.

High male incidence and evolutionary implications of triploid form in northeast Asia Carassius auratus complex

“…(Vasil'ev et al, 2003), Misgurnus anguillicaudatus (Itono et al, 2006), and their fertile function was revealed in unisexual Squalius alburnoides (Sousa-Santos et al, 2007) and Poecilia formosa (Lamatsch et al, 2010). In the triploid form of Carassius auratus complex, approximate 1-10% of triploid males were sporadically reported in natural habitats (Gui and Zhou, 2010), but the unusually triploid male incidence of high up to 23% should be firstly discovered in the gynogenetic triploid form. What are the reasons for the existence and high incidence of triploid males in the triploid form of Carassius auratus complex?…”

“…In the past, genetic evidence of sexual reproduction in triploid males has been demonstrated by experimental propagation and genetic marker analysis under captive condition (Gui and Zhou, 2010), but their ecologically genetic roles have remained unknown in natural habitats. In the present study, we utilized the existence difference of a relatively ubiquitous mtDNA CR2 haplotype in triploid females and triploid males to analyze the proportional relationship of triploids and triploid males with this haplotype in the four surveyed populations, and revealed the genetic evidence that sexual reproduction between triploid males and triploid females might have been performed in natural triploid form of the northeast Asia Carassius auratus complex.…”

“…Carassius auratus complex has been generally thought to consist of both diploid form and triploid form that cannot be discriminated morphologically from each other (Apalikova et al, 2011;Gui and Zhou, 2010;Jakovlić and Gui, 2011;Takada et al, 2010), even though tetraploidization has been demonstrated to occur in the diploid form with 100 chromosomes (Ohno et al, 1967), and evolutionary hexaploid has been also suggested for the triploid form with more than 150 chromosomes (Zhou and Gui, 2002;Zhu et al, 2006). According to the current taxonomic category, the triploid form, also commonly known as gibel carp, silver crucian carp or Prussian carp, has been recognized as a subspecies gibel carp Carassius auratus gibelio (Cherfas, 1981;Jiang et al, 1983) of Carassius auratus, including the domestic goldfish, or even a separate species Carassius gibelio (Kalous et al, 2007;Kalous and Martin, 2011;Rylková et al, 2010).…”

“…Recently, along with cytogenetic and molecular marker development, it has been extensively observed in many countries of the Eurasian continent, such as in Britain, Italy, Germany (Hänfling et al, 2005), Hungary (Tóth et al, 2005), Greece (Liousia et al, 2008), Czech Republic (Kalous et al, 2007;Veteŝník et al, 2007), Kazakhstan (Sakai et al, 2009), and Croatia (Jakovlić and Gui, 2011). In the past decade, a lot of genetic knowledge including molecular basis of reproduction trait and numerous polymorphic DNA markers has been investigated and characterized from the triploid form (Gui and Zhou, 2010;Gui and Zhu, 2012). Similar to other polyploid salamanders, frogs and fish (Lampert and Schartl, 2010;Schlupp, 2005;Stöck et al, 2012), the triploid form can also reproduce by sperm-dependent gynogenesis, and many diverse gynogenetic clones have been discriminated by different genetic markers, such as transferrin Yang et al, 2001, RAPD and SCAR markers (Zhou et al, 2001(Zhou et al, , 2000b, microsatellite (Guo and Gui, 2008) and mtDNA sequence (Apalikova et al, 2008;Brykov et al, 2005;Li and Gui, 2008).…”

“…Similar to other polyploid salamanders, frogs and fish (Lampert and Schartl, 2010;Schlupp, 2005;Stöck et al, 2012), the triploid form can also reproduce by sperm-dependent gynogenesis, and many diverse gynogenetic clones have been discriminated by different genetic markers, such as transferrin Yang et al, 2001, RAPD and SCAR markers (Zhou et al, 2001(Zhou et al, , 2000b, microsatellite (Guo and Gui, 2008) and mtDNA sequence (Apalikova et al, 2008;Brykov et al, 2005;Li and Gui, 2008). Interestingly, a minor but significant portion (approx 1-10%) of triploid males were found in the triploid form, and normal sperm production and their sexual reproduction ability have been demonstrated by experimental propagation and genetic analysis in the triploid form (Gui and Zhou, 2010;Peng et al, 2009;Sun et al, 2010;Zhou et al, 2000a). Moreover, a novel nucleo-cytoplasmic hybrid clone was synthesized from the sexual reproduction mating between clone D female and clone A male, and it was suggested through genetic analysis to arise via androgenesis by a mechanism of ploidy doubling of clone A sperm in clone D ooplasm through inhibiting the first mitotic division (Wang et al, 2011).…”