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

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.

Sequence capture: Obsolete or irreplaceable? A thorough validation across phylogenetic distances and its applicability to hybrids and allopolyploids

“…Genomic analyses of such organisms bring new insights into the mechanisms of genome evolution (e.g. Lu et al, 2022; Yoo et al, 2014) and SEQcap methodologies have indeed been employed to study phenomena like structural variations or loss of heterozygosity (e.g. Mu et al, 2019; Westphalen et al, 2022).…”

Deciphering male influence in gynogenetic Pengze crucian carp (Carassius auratus var. pengsenensis): insights from Nanopore sequencing of structural variations

“…The observed variation indicates the emergence of novel SVs, which may result from a variety of mechanisms. These include sporadic homologous recombination and high-frequency gene conversion during the maturation of oocytes ( Wang et al, 2022 ), the suppression of DNA double-strand break formation and homologous recombination in oocytes ( Lu et al, 2022 ), or the incorporation of male genetic fragments during the gynogenetic process ( Zhang et al, 1999 ; Zhao et al, 2004a ; Mao et al, 2020 ; Ding et al, 2021 ; Zhao et al, 2021 ). The process of recombination, depending on its accuracy, plays a dual role: inaccurate recombination can lead to the introduction of new genetic variations, whereas precise recombination has the potential to correct existing genetic errors ( Burssed et al, 2022 ).…”

“…Remarkably, the range of DSVs observed in offspring remained consistently within 2.2%–2.7%, regardless of the sperm stimulation method applied. Drawing on cytological evidence of sporadic homologous recombination and reduced double-strand break repair in oocytes ( Lu et al, 2022 ; Wang et al, 2022 ), it appears that DSVs, rather than being male-specific, may primarily result from both accurate and inaccurate homologous recombination processes, whereas MSSVs are derived from male genetic contributions. Notably, under homologous sperm stimulation, the proportion of DSVs classified as MSSVs (21.4% to 23.2%) significantly surpassed that observed with heterologous sperm stimulation (4.3% to 5.3%).…”

Can changes in ploidy drive the evolution to allogamy in a selfing species complex?

“…Instead, the pattern of genomic diversity observed in this study could be supported by the occurrence of outcrossing events in these populations. Recent studies in other polyploid species complexes have underlined the effects of the mating system and ploidy changes on genomic diversity (Lu et al ., 2022). In our system, genomic diversity increased in higher ploidy levels.…”