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.
Highlights
Sexual reproduction is prevalent in vertebrates, while only about 100 taxa have been documented to develop unisexual reproductive ability [1,2,3] since the first unisexual vertebrate Amazon molly (Poecilia formosa) was described in 1932 [4,5]
The unassembled sequence of C. gibelio and C. auratus genome generated in this study have been submitted to the NCBI BioProject database under accession number PRJNA659101
The PacBio-SMRT data of the three male-specific microchromosomes generated in this study have been submitted to the NCBI BioProject database under accession number PRJNA658923, PRJNA658930, and PRJNA658940
Summary
Sexual reproduction is prevalent in vertebrates, while only about 100 taxa have been documented to develop unisexual reproductive ability [1,2,3] since the first unisexual vertebrate Amazon molly (Poecilia formosa) was described in 1932 [4,5]. Unisexual vertebrates produce solely female offspring with nearly identical genetic information, mainly via three modes including parthenogenesis, gynogenesis, or hybridogenesis [2,3,6]. Females produce unreduced eggs containing the same chromosome complement as somatic cells, and these eggs develop into offspring spontaneously in the absence of males [7]. Females produce unreduced eggs with the same chromosome complement as somatic cells, but sperm are required to stimulate the eggs to initiate embryogenesis using only maternal genetic information [8]. Females produce reduced eggs that contain only maternal haploid chromosomes, and these eggs must be fertilized by sperm from another species. These hybridogenetic offspring contain both maternal and paternal haploid chromosomes, but only maternal haploid chromosomes remain in the reduced eggs [9]
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