The origin and maintenance of unisexual vertebrates have long fascinated evolutionary biologists. Traditionally, unisexual lineages have been predicted to be evolutionarily short-lived. Due to the absence of normal meiosis, clonal lineages lack recombinational genetic variation and accumulate deleterious mutations, which inevitably lead to genomic decay. Intriguingly, most unisexual vertebrate species usually live in sympatric association with their bisexual diploid relatives and form sexual diploid–unisexual polyploid complexes. Some of the unisexual vertebrates have evolved for more than several hundred thousand years and have successfully colonized wider and harsher habitats than their sexual relatives. However, their strategy for avoiding genomic decay remains unclear.   

Recently, a research team led by Prof. GUI Jianfang from the Institute of Hydrobiology (IHB) of the Chinese Academy of Sciences provided comprehensive evidence that ploidy changes, drive unisexual and sexual reproduction transition, thereby leading to genomic and clonal diversity in the polyploid Carassius species complex. The study was published in Molecular Biology and Evolution.   

The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian carp or goldfish) (AABB) and the gynogenetic amphitriploid C. gibelio (gibel carp) (AAABBB). Subsequently, the researchers developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome.    

In this study, the researchers generated novel amphitriploids (AAABBB) by backcrossing the amphitetraploid male with the amphidiploid C. auratus. Whole-genome resequencing revealed the genomic changes, including recombination and independent assortment between homologs of C. gibelio and C. auratus. These changes lead to high genomic diversity in novel amphitriploids.   

The researchers further investigated the fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte were discovered, and their distinct development fates were observed. Type I oocytes entered apoptosis due to improper synaptonemal complex assembly and incomplete double-strand break repair, whereas subsequent type II oocytes bypassed meiosis through an alternative ameiotic pathway to develop into mature eggs, similar as C. gibelio.   

Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced.   

This study uncovers an efficient strategy for generating diverse clonal lineages in polyploid Carassius complex, which may enable gynogenetic Carassius avoid genomic decay and increase the potential evolvability. Meanwhile, the researchers create diverse genetic clones and exploit a promising approach for precise genetic breeding of C. gibelio. 

Schematic diagram for sexual reproduction (meiosis) and unisexual gynogenesis (ameiotic pathway) transition and clonal diversity driven via ploidy changes in Carassius complex. NA3n, novel amphitriploid; GA3n, gynogenetic amphitriploid; CA3n, cloned amphitriploid; ♀, female; ♂, male. (Figure by IHB) 

(Editor: MA Yun)