Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from Cobitis taenia Complex

Abstract

The transition from sexual reproduction to asexuality is often triggered by hybridization. The gametogenesis of many hybrid asexuals involves premeiotic genome endoreplication leading to bypass hybrid sterility and forming clonal gametes. However, it is still not clear when endoreplication occurs, how many gonial cells it affects and whether its rate differs among clonal lineages. Here, we investigated meiotic and premeiotic cells of diploid and triploid hybrids of spined loaches (Cypriniformes: Cobitis) that reproduce by gynogenesis. We found that in naturally and experimentally produced F1 hybrids asexuality is achieved by genome endoreplication, which occurs in gonocytes just before entering meiosis or, rarely, one or a few divisions before meiosis. However, genome endoreplication was observed only in a minor fraction of the hybrid’s gonocytes, while the vast majority of gonocytes were unable to duplicate their genomes and consequently could not proceed beyond pachytene due to defects in bivalent formation. We also noted that the rate of endoreplication was significantly higher among gonocytes of hybrids from natural clones than of experimentally produced F1 hybrids. Thus, asexuality and hybrid sterility are intimately related phenomena and the transition from sexual reproduction to asexuality must overcome significant problems with genome incompatibilities with a possible impact on reproductive potential.

Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus

“…Moreover, in water frogs cell cycle and even meiotic checkpoint seems to be not very strict as aneuploid and mispaired chromosomes in meiosis are able to proceed at least to diplotene stage in case of females (Dedukh et al, 2015;Dedukh et al, 2017;Dedukh et al, 2019) and to aneuploid primary spermatocytes and gametes in case of males [this study (Doležálková et al, 2016;Pustovalova et al, 2022)]. In diploid and triploid gynogenetic fish females in Cobitis taenia complex as well as parthenogenetic geckos (Dedukh et al, 2021;Dedukh et al, 2022a), only a small fraction (1.5%-11%) of oogonia has correctly endoreplicated genome allowing them to achieve diplotene stage. Nevertheless, the majority of oogonia failed to proceed beyond pachytene due to errors in bivalent formation and inability to pass the cell cycle checkpoints.…”

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

“…Through interploidy hybridization, the produced novel amphitriploids return to triploidization and successively form two types of oocyte. Similarly, in naturally and experimentally produced F1 hybrids of unisexual Cobitis , two types of pachytene oocyte were observed, in which the vast majority (>95%) of oocytes containing a mixture of bivalents and univalents failed to develop further, whereas only the remaining oocytes formed double bivalents via premeiotic endoreplication and finally completed meiosis ( Dedukh et al 2021 ). Based on these observations, Dedukh et al (2021) proposed that a pachytene checkpoint that involves DSB repair machinery ( Roeder and Bailis 2000 ; Subramanian and Hochwagen 2014 ) might prevent developmental progression of the vast majority of oocytes and lead to their death.…”

“…Similarly, in naturally and experimentally produced F1 hybrids of unisexual Cobitis , two types of pachytene oocyte were observed, in which the vast majority (>95%) of oocytes containing a mixture of bivalents and univalents failed to develop further, whereas only the remaining oocytes formed double bivalents via premeiotic endoreplication and finally completed meiosis ( Dedukh et al 2021 ). Based on these observations, Dedukh et al (2021) proposed that a pachytene checkpoint that involves DSB repair machinery ( Roeder and Bailis 2000 ; Subramanian and Hochwagen 2014 ) might prevent developmental progression of the vast majority of oocytes and lead to their death. In the novel amphitriploids observed in the present study, type I oocytes gave priority to meiosis from sexual C. auratus , in which ∼50 SC bivalents were assembled, but the DSBs on the other unsynapsed 50 chromosomes were not completely repaired ( fig.…”

Achiasmatic meiosis in the unisexual Amazon molly, Poecilia formosa

“…Nevertheless, in contrast to P. formosa , in C. gibelio , chromosomal pairing and recombination have been observed at least between some homologous chromosomes (Zhang et al 1992 ). In other asexuals exploiting endoreplication, only oocytes with normal pairing were able to proceed beyond pachytene while oocytes with aberrant pairing were filtered out at pachytene (Dedukh et al 2021 , 2022 ). In zebrafish, the mutants with non-functional Mlh1 and Spo11 have different outcomes depending on their sex: males are sterile and produce no sperm while mutant females are fertile, yet produce malformed progeny that fails to develop, likely due to severe aneuploidy (Feitsma et al 2007 ; Leal et al 2008 ; Blokhina et al 2019 ).…”

“…In zebrafish, the mutants with non-functional Mlh1 and Spo11 have different outcomes depending on their sex: males are sterile and produce no sperm while mutant females are fertile, yet produce malformed progeny that fails to develop, likely due to severe aneuploidy (Feitsma et al 2007 ; Leal et al 2008 ; Blokhina et al 2019 ). However, in F1 hybrids of medaka and Cobitis , males exhibit aberrant pairing during pachytene, but chromosomes can proceed beyond pachytene until metaphase of meiosis I (Shimizu et al 1997 ; Dedukh et al 2020 , 2021 ). On the contrary, in female hybrids, pachytene cells which exhibit aberrant pairing cannot proceed beyond pachytene to diplotene, thus indirectly indicating the pachytene checkpoint in females (Shimizu et al 2000 ; Dedukh et al 2021 ).…”