Abstract
BackgroundCoexistence and transition of diverse sex determination strategies have been revealed in some ectothermic species, but the variation between males caused by different sex determination strategies and the underlying mechanism remain unclear. Here, we used the gynogenetic gibel carp (Carassius gibelio) with both genotypic sex determination (GSD) and temperature-dependent sex determination (TSD) strategies to illustrate this issue.ResultsWe found out that males of GSD and TSD in gibel carp had similar morphology, testicular histology, sperm structure and sperm vitality. However, when maternal individuals were mated with males of GSD, sperm nucleus swelling and fusing with the female pronucleus were observed in the fertilized eggs. On the contrary, when maternal individuals were mated with males of TSD, sperm nucleus remained in the condensed status throughout the whole process. Subsequently, semen proteomics analysis unveiled that DNA replication and gene expression-related pathways were inhibited in the sperm from males of TSD compared to males of GSD, and most differentially expressed proteins associated with DNA replication, transcription and translation were down-regulated. Moreover, via BrdU incorporation and immunofluorescence detection, male nucleus replication was revealed to be present in the fertilized eggs by the sperm from males of GSD, but absent in the fertilized eggs by the sperm from males of TSD.ConclusionsThese findings indicate that DNA replication and gene expression-related pathways are associated with the distinct sperm nucleus development behaviors in fertilized eggs in response to the sperm from males of GSD and TSD. And this study is the first attempt to screen the differences between males determined via GSD and TSD in gynogenetic species, which might give a hint for understanding evolutionary adaption of diverse sex determination mechanisms in unisexual vertebrates.
Highlights
Coexistence and transition of diverse sex determination strategies have been revealed in some ectothermic species, but the variation between males caused by different sex determination strategies and the underlying mechanism remain unclear
Structure, vitality, and hatchability To reveal similarities and differences between the sperm from males of genotypic sex determination (GSD) and temperature-dependent sex determination (TSD), we firstly examined the sperm morphology under scanning electron microscope (SEM) and both types of sperm had normal morphology that a flagellum came from the basal body (Fig. 2a and d)
The sperm structure with nucleus (N), mid-piece (M) and flagellum (F) were observed (Fig. 2b and e), and the flagellum composed of 9 doublet microtubules and 2 central microtubules were detected in both males of GSD and TSD (Fig. 2c and f) under transmission electron microscopy (TEM)
Summary
Coexistence and transition of diverse sex determination strategies have been revealed in some ectothermic species, but the variation between males caused by different sex determination strategies and the underlying mechanism remain unclear. While individuals with ESD do not have genetic difference between sexes, and their sex is determined during development [4] via environmental factors including temperature [5], photoperiod [6], social factors [7], pH and dissolved oxygen (DO) [8] These two seemingly distinct sex determination strategies are not mutually exclusive, and coexistence, interaction and transition of GSD and ESD have been observed in fishes [9, 10], amphibians [11] and reptiles [5]. Compared with other unisexual vertebrates [16], rare but significant male incidences were observed in many natural habitats [9, 17, 18] of gibel carp with unisexual gynogenetic ability [17, 19, 20] Both GSD and temperature-dependent sex determination (TSD) were found to coexist in gibel carp through analyses of natural populations and lab experimental progenies [9, 21]. Diverse sex determination mechanisms of GSD and TSD [9, 21] and dual reproduction modes including unisexual gynogenesis and sexual reproduction [17, 19, 20] make gibel carp an ideal system to investigate plastic sex determination strategies and their evolutionary consequences
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