Genome Anatomy of Amphitriploid Gibel Carp Reveals Evolutionary Insights into Unisexual Reproductive Success

 Amphidiploid and amphitriploid (Credit: IHB) 

Unisexual reproduction lacks the meiotic recombination, resulting in the accumulation of deleterious mutations and hindering the creation of genetic diversity. Thus, unisexual taxa are commonly considered an evolutionary dead end. Intriguingly, some unisexual fishes and reptiles have outlived their predicted extinction time and exhibited high genetic diversity and strong environmental adaptation, yet evolutionary mechanisms underlying unisexual reproductive success remain unclear in these vertebrates.    

Recently, a collaborative study led by Prof. GUI Jianfang from Institute of Hydrobiology, Chinese Academy of Sciences, Prof. WANG Wen from Northwestern Polytechnical University, Prof. FANG Xiaodong from BGI-Shenzhen, revealed the evolutionary puzzle of unisexual reproductive success in hexaploid gynogenetic gibel carp (Carassius gibelio). This study was published in Nature Ecology & Evolution.   

In this study, the research team sequenced the genomes of sexual tetraploid crucian carp (C. auratus) and unisexual hexaploid gibel carp (C. gibelio) and assembled their haplotypes to chromosome level. Both haplotypes have 50 chromosomes, which are composed of two subgenomes (25 chromosomes from subgenome A and 25 chromosomes from subgenome B).    

Sequencing coverage analysis reveals that tetraploid C. auratus is an amphidiploid (AABB) with two diploid sets of chromosomes and hexaploid C. gibelio is an amphitriploid (AAABBB) with two triploid sets of chromosomes.   

Based on the resequencing data from different strains of C. auratus and C. gibelio, the research team demonstrated that amphitriploid C. gibelio originated from ancestral amphidiploid C. auratus via autotriploidy in about 0.82-0.96 million years ago. The amphitriploid C. gibelio has overcome the meiotic obstacle caused by three homologous chromosomes through unisexual gynogenesis.    

Through comparative genomics, the researchers identified intensive expansion and alterations of meiotic cell cycle-related genes and an oocyte-specific histone variant in C. gibelio, and found out that most of these expanded genes showed high expression in ovaries and oocytes.    

Besides, the research team found that C. gibelio produces unreduced oocytes by suppressing meiosis I. However, sporadic homologous recombination and a high rate of gene conversion were revealed during oogenesis of C. gibelio. These genomic changes might have facilitated purging deleterious mutations and maintaining genome stability in amphitriploid C. gibelio.   

This research assembled and characterized the first amphitriploid genome, providing novel insights into the evolutionary mechanisms of the reproductive success in unisexual polyploid vertebrates. 

(Editor: MA Yun)