Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Meng Lu; Zhi Li; Zi-Yu Zhu; Fang Peng; Yang Wang; Xi-Yin Li; Zhong-Wei Wang; Xiao-Juan Zhang; Li Zhou; Jian-Fang Gui

doi:10.1093/molbev/msac188

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Mol Biol Evol. 2022 Sep 1;39(9):msac188. doi: 10.1093/molbev/msac188.

Authors

Meng Lu^{1

2}, Zhi Li^{1

2}, Zi-Yu Zhu^{1

2}, Fang Peng^{1

2}, Yang Wang^{1

2}, Xi-Yin Li^{1

2}, Zhong-Wei Wang^{1

2}, Xiao-Juan Zhang^{1

2}, Li Zhou^{1

2}, Jian-Fang Gui^{1

2}

Affiliations

¹ State Key Laboratory of Freshwater Ecology and Biotechnology, Hubei Hongshan Laboratory, the Innovation Academy of Seed Design, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China.
² University of Chinese Academy of Sciences, Beijing 100049, China.

Abstract

Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. 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). Recently, we developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome. In this study, we 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. The fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids were investigated. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte (with and without homolog synapsis) 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. Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced. These revealed genomic changes and detailed cytological data provide comprehensive evidence that changes in ploidy drive unisexual and sexual reproduction transition, thereby resulting in genomic diversity and allowing C. gibelio avoid genomic decay.

Keywords: clonal diversity; genomic decay; meiosis; polyploid Carassius complex; reproduction transition; unisexual reproduction.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Carps*
Female
Genomics
Male
Ploidies
Polyploidy*
Reproduction / genetics