Genomic anatomy of male-specific microchromosomes in a gynogenetic fish

Abstract

Unisexual taxa are commonly considered short-lived as the absence of meiotic recombination is supposed to accumulate deleterious mutations and hinder the creation of genetic diversity. However, the gynogenetic gibel carp (Carassius gibelio) with high genetic diversity and wide ecological distribution has outlived its predicted extinction time of a strict unisexual reproduction population. Unlike other unisexual vertebrates, males associated with supernumerary microchromosomes have been observed in gibel carp, which provides a unique system to explore the rationales underlying male occurrence in unisexual lineage and evolution of unisexual reproduction. Here, we identified a massively expanded satellite DNA cluster on microchromosomes of hexaploid gibel carp via comparing with the ancestral tetraploid crucian carp (Carassius auratus). Based on the satellite cluster, we developed a method for single chromosomal fluorescence microdissection and isolated three male-specific microchromosomes in a male metaphase cell. Genomic anatomy revealed that these male-specific microchromosomes contained homologous sequences of autosomes and abundant repetitive elements. Significantly, several potential male-specific genes with transcriptional activity were identified, among which four and five genes displayed male-specific and male-biased expression in gonads, respectively, during the developmental period of sex determination. Therefore, the male-specific microchromosomes resembling common features of sex chromosomes may be the main driving force for male occurrence in gynogenetic gibel carp, which sheds new light on the evolution of unisexual reproduction.

Structural Abnormalities of Spermatozoa in Triploid Gynogenetic Crucian Carp (Carassius auratus)

“…Gynogenesis fish often are not dependent on the involvement of sperm genetic material, in which the sperms are required to stimulate the eggs to initiate embryogenesis using only maternal genetic information (Gui and Zhou 2010). The introgression of paternal DNA might play an important role in the creation of genetic diversity in gynogenetic fish, for example, extra microchromosomes in males are closely related to male determination in gynogenetic gibel carp (Li et al, 2016;Zhao et al, 2021;Ding et al, 2021), and the insertion of paternal DNA was also reported in gynogenetic blunt snout bream (Gong et al, 2019). 3nDTCC is generally propagated by gynogenesis.…”

Fish female-biased gene cyp19a1a leads to female antiviral response attenuation between sexes by autophagic degradation of MITA

“…The gibel carp individuals used for experiments were about 2.5 months post hatching (3 ± 1 g). The breeding and maintenance of gibel carp were performed as previously described [40]. All fish were maintained according to institutional and national ethical and animal welfare guidelines in the laboratory for at least two weeks prior to the experiments for acclimatization and evaluation of overall fish health.…”

Two duplicated gsdf homeologs cooperatively regulate male differentiation by inhibiting cyp19a1a transcription in a hexaploid fish

“…To uncover the function of gsdf in male development, we performed loss-of-function analysis using CRISPR/Cas9 in the hexaploid C. gibelio with three alleles of gsdf-A and three alleles of gsdf-B. were injected into the fertilized eggs between a WT female gibel carp without MSM (MSM−) (P: parental generation) and a male common carp to initiate typical gynogenesis [32][33][34][35]. All the individuals of the G0 generation were females (MSM−) with gsdf-A chimeric mutations For gsdf-A potential promoter, the transcriptional regulation ability of Dmrt1-A was significantly stronger than that of Dmrt1-B.…”

“…When a female gibel carp is mated with a genotypic amphitriploid male, a variant of gynogenesis is initiated, during which the sperm nuclei are also extruded but some supernumerary microchromosomes of sperm nuclei occasionally leak into the unreduced eggs. This variant of gynogenesis can accumulate microchromosomes, generate males, and create genetic diversity in the offspring [32][33][34][35]. However, details concerning the molecular mechanism of male determination and differentiation in this gynogenetic hexaploid fish are limited.…”