Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Abstract

Formation of species generally occurs in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report that speciation proceeds through a previously unnoticed stage at which gene flow is completely interrupted on side of both hybrid's sexes, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to the formation of clonal gametes. Specifically, analysis of gametogenetic pathways in hybrids between fish species Cobitis elongatoides and C. taenia revealed that male HS resulted from extensive asynapses and crossover reduction among elongatoides-taenia chromosomal pairs followed by apoptosis. By contrast, hybrid females exhibited premeiotic genome endoreplication which ensured proper formation of bivalents between identical chromosomal copies. This deviation ultimately restored fertility in females but since it simultaneously leads to the production of unreduced clonal gametes, it restricts interspecific gene flow thereby directly contributing to speciation. In conclusion, our data demonstrate that the emergence of asexuality may remedy HS in a sex-specific manner and is intermingled with the speciation process. Although gametogenetic mechanisms employed by asexual animals and plants have rarely been scrutinized, available evidence suggests that premeiotic endoreplication is relatively widespread. This suggests that observed link between HS and clonality may have general validity in taxa able of asexual reproduction. Author's summarySpecies are fundamental evolutionary units that presumably evolve in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report the existence of a previously unnoticed stage of speciation at which gene flow is completely interrupted, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to formation of clonal gametes. Specifically, HS resulted from extensive asynapses in male gonads, but in females the hybridization provoked premeiotic endoreplication which rescued chromosome pairing and fertility. Simultaneously, this meiotic deviation caused clonal transmission of maternal genome, thereby effectively restricting the interspeficic gene flow. Our results emphasize that emergence of clonality is a type of hybrid incompatibility that is intermingled with the formation of b...

Genome fractionation and loss of heterozygosity in hybrids and polyploids: mechanisms, consequences for selection, and link to gene function

“…Hence, even if ectopic ExT pairings occur in cells of asexual females, the formation of proper bivalents would be unlikely and gametes would not be formed. Second, (Dedukh et al 2020) documented the occurrence of true COs in ExE and TxT bivalents in hybrid females (Fig. 1a) suggesting that hypothetical ExT bivalents would result in the exchange of large pieces of chromosomal arms, which was not observed (Majtánová et al 2016).…”

“…Interestingly, it is unclear how such conversions between orthologs may arise since organisms employing premeiotic endoreplication should rather form bivalents between sister copies of the duplicated homologs (Lutes et al 2010;Arai and Fujimoto 2013;Dedukh et al 2020) (Fig. 1a).…”

“…In theory, they may result from errors in homology search during early meiosis if ExT bivalents are formed, but this explanation is unlikely for two reasons. First, C. elongatoides and C. taenia karyotypes are so divergent that most orthologous chromosomes may not form proper bivalents, leading to sterility of hybrid forms that lack endoreplication, typically males (Dedukh et al 2020). Hence, even if ectopic ExT pairings occur in cells of asexual females, the formation of proper bivalents would be unlikely and gametes would not be formed.…”

“…Note that the latter case may cause loss of heterozygosity among progeny via crossovers or gene conversions. Insert on the right demonstrates empirical evidence for the presence of proper bivalents in hybrid's oocytes as from (Dedukh et al 2020). b) Reproduction scheme of Cobitis; letters correspond to haploid genomes: E = C. elongatoides, T = C. taenia.…”

“…However, with ongoing divergence, these species lost the capacity to produce sexual hybrids as crossings of the current species led to sterile hybrid males but clonally reproducing, fertile hybrid females. Hybrid females form unreduced gametes by premeiotic endoduplication but are gynogenetic, i.e., they require sperm from a sexual species to trigger development of their gametes (Janko et al 2007;Choleva et al 2012;Dedukh et al 2020).…”