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.

Highlights

  • Since the first unisexual fish, the Amazon molly Poecilia formosa, was found in 193213, about 90 all-female unisexual complexes have been reported in fish, amphibians and reptiles[6,14]

  • Through a series of studies for more than 10 years, our laboratory has identified some important genes involved in oogenesis, oocyte maturation and egg fertilization from the polyploid fish[45,46,47,48,49], and found that a significant maternal-effect factor Spindlin, which localizes on meiotic spindle[49], might be a useful molecular marker for elaborating regulative mechanism of the unique multiple reproduction modes

  • To investigate whether normal meiosis was completed in clone D of Carassius gibelio, we collected different stage maturing oocytes and mature eggs from the artificial induction spawning females

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Summary

Introduction

Since the first unisexual fish, the Amazon molly Poecilia formosa, was found in 193213, about 90 all-female unisexual complexes have been reported in fish, amphibians and reptiles[6,14] These unisexual animals have been demonstrated to reproduce by gynogenesis, hybridogenesis, parthenogenesis, or kleptogenesis[8,10,15,16], but how to restore the exact chromosome number and genome ploidy level and how to maintain the genetic diversity for adapting to variable environments have remained unclear. Commonly known as Prussian carp, silver crucian carp or gibel carp, named as a subspecies Carassius auratus gibelio of Carassius auratus[8,18,19], was preliminarily found to be able to reproduce by unisexual reproduction of gynogenesis early in the last century[8] It has diverse karyotypes with 156 or 162 chromosomes[20], and genome reshuffling, chromosome and chromosomal fragment incorporation have occurred by manipulation or mating between various clones[21]. We aim to utilize the spindle localization of β -tubulin and Spindlin to trace the meiosis process, and attempt to use DAPI staining as well as BrdU incorporation and immunofluorescence detection to reveal dynamic development progresses and early embryonic cleavage changes between different reproduction modes

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