Genomic anatomy of male-specific microchromosomes in a gynogenetic fish

Author summary Unisexual taxa are considered short-lived as the accumulation of deleterious mutations and hindering the creation of genetic diversity. However, the gynogenetic gibel carp (Carassius gibelio) containing rare and variable proportions of males in wild populations has outlived its predicted time of extinction and exhibited strong environmental adaptation, which provides a special system to investigate the evolution of unisexual reproduction in vertebrates. Our previous studies have revealed that the supernumerary microchromosomes are associated with male determination in gibel carp. Here, we further isolated three male-specific supernumerary microchromosomes and revealed that they contained homologous sequences of autosomes and abundant repetitive elements. Besides, we identified several genes with transcriptional activity on these microchromosomes, especially some genes with male-specific or male-biased expression during the developmental period of sex determination. The male-specific microchromosomes with abundant repetitive elements and active male-specific/male-biased genes display common features of sex chromosomes and may be the main driving forces for male occurrence in gynogenetic gibel carp. 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.

Automated summary

Unisexual taxa are often considered short-lived due to the accumulation of deleterious mutations caused by the absence of meiotic recombination. However, the gynogenetic gibel carp has shown exceptional longevity and strong environmental adaptation. Male occurrence in this species is associated with male-specific microchromosomes containing homologous sequences of autosomes and abundant repetitive elements, which are likely the main driving force for male occurrence in gynogenetic gibel carp.