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 a stage of premeiotic genomic endoreduplication leading to the production of clonal gametes and bypassing genomic incompatibilities that would normally cause hybrid sterility. However, it is still not clear at what gametogenic stage the 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 naturally as well as experimentally produced F1 hybrid strains undergo an obligatory genome duplication event to achieve asexuality, occurring in the gonocytes just before entering meiosis or, rarely, one or few divisions before meiosis. Surprisingly, however, the genome endoreplication was observed only in a minor fraction of the hybrid's gonocytes, while the vast majority were unable to duplicate their genomes and consequently could not proceed beyond pachytene due to defects in pairing and bivalent formation. We also noted that the rate of endoreplication was significantly higher among gonocytes of hybrids from successful natural clones than of experimentally produced F1 hybrids, indicating that interclonal selection may favor lineages that maximize the rate of premeiotic endoreduplication. We conclude that asexuality and hybrid sterility are intimately related phenomena and the transition from sexual reproduction to asexuality must overcome significant problems with genome incompatibilities with possible impact on reproductive potential.

Genetic and karyotype divergence between parents affect clonality and sterility in hybrids

“…The contrasting incidence of oocytes with endoreplicated genomes between pachytene (aprox 6 %) and diplotene stages (100%) is consistent with previous results 27 suggesting that premeiotic genome endoreplication is a rare event in all types of crosses. This allows cells to form normal bivalents and to enter the diplotene, while the majority of cells remain non-duplicated and cannot proceed beyond the pachytene checkpoint due to mispairing among orthologous chromosomes.…”

“…S8a-e). Similar to previous data on natural clones 13,27 , we therefore conclude that diplotene oocytes in the majority of hybrid females contain only cells with duplicated genomes, suggesting their ability to complete clonal gametogenesis (Fig. 4; Supplementary Fig.…”

“…2, Fig. 6) and it has also been reported from several natural hybrid complexes 13,15,27 . An intermediate situation was observed in TP-hybrids between a closely related species that diverged ~1 Mya 17 , where males produced reduced gametes and females produced both, reduced and unreduced ones.…”

“…We therefore treated all experimental progenies as a single group and tested whether they differed from previously-analysed natural diploid ET-hybrids, whose incidence of duplicated gonocytes was higher, on average ~6%; 27 . Here, the difference was significant (Wald Z-test of GLMM; DF = 1; p-value = 0.0067), suggesting that natural clones produce a higher proportion of oocytes with endoreplicated genomes than experimetal F1 hybrids.…”

“…1b), 26 . In these natural systems, only hybrid females are known to produce unreduced gametes, employing premeiotic genome endoreplication, while hybrid males are usually sterile due to aberrant pairing of chromosomes in meiosis 15,27 .…”